Skip to main content
Log in

Pantoea tagorei sp. nov., a Rhizospheric Bacteria with Plant Growth-Promoting Activities

  • ORIGINAL RESEARCH ARTICLE
  • Published:
Indian Journal of Microbiology Aims and scope Submit manuscript

Abstract

A Gram-negative, short-rod, non-motile, facultatively anaerobic, potassium-solubilizing bacterium MR1 (Mine Rhizosphere) was isolated from rhizospheric soil of an open-cast coal mine of Jharia, Jharkhand, India. Isolate MR1 can grow in a broad range of temperature, pH, and NaCl concentrations. The 16S rRNA gene sequence of the strain showed 99.24% similarity with Pantoea septica LMG 5345T. However, maximum-likelihood tree constructed using 16S rRNA gene sequence, multilocus sequence analysis using concatenated sequences of ten housekeeping genes, whole-genome based phylogenetic reconstruction, digital DNA–DNA hybridization, and average nucleotide identity (ANIm and ANIb) values indicated segregation of MR1 from its closest relatives. Fatty acid profile of MR1 also suggested the same, with clear variation in major and minor fatty acid contents, having C13:0 anteiso (10-Methyldodecanoic acid) as the unique one. Thus, considering all polyphasic data, strain MR1T (= MTCC 13265T, where ‘T’ stands for Type strain) is presented as a novel species of the genus Pantoea, for which the name Pantoea tagorei sp. nov. is proposed.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The Whole Genome sequence has been deposited at DDBJ/ENA/GenBank under the Bioproject accession PRJNA892926.

Abbreviations

WGS:

Whole-genome sequencing

MLSA:

Multilocus sequence analysis

TYGS:

Type Strain Genome Server

dDDH:

Digital DNA–DNA hybridization

FAME:

Fatty acid methyl ester

References

  1. Gavini F, Mergaert J, Beji A, Mielcarek C, Izard D, Kersters K, De Ley J (1989) 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 39:337–345

    Google Scholar 

  2. Cruz AT, Cazacu AC, Allen CH (2007) Pantoea agglomerans, a plant pathogen causing human disease. J Clin Microbiol 45:1989–1992

    Article  PubMed  PubMed Central  Google Scholar 

  3. Prakash O, Nimonkar Y, Vaishampayan A, Mishra M, Kumbhare S, Josef N, Shouche YS (2015) Pantoea intestinalis sp. nov., isolated from the human gut. Int J Syst Evol Microbiol 65:3352–3358

    Article  CAS  PubMed  Google Scholar 

  4. Bomfeti CA, Souza-Paccola EA, Massola Júnior NS, Marriel IE, Meirelles WF, Casela CR, Paccola-Meirelles LD (2008) Localization of Pantoea ananatis inside lesions of maize white spot disease using transmission electron microscopy and molecular techniques. Trop Plant Pathol 33:63–66

    Article  Google Scholar 

  5. Abidin N, Ismail SI, Vadamalai G, Yusof MT, Hakiman M, Karam DS, Ismail-Suhaimy NW, Ibrahim R, Zulperi D (2020) Genetic diversity of Pantoea stewartii subspecies stewartii causing jackfruit-bronzing disease in Malaysia. PLoS ONE 15:1–18

    Article  Google Scholar 

  6. Merbach W, Ruppel S, Schulze J (1998) Dinitrogen fixation of microbe-plant associations as affected by nitrate and ammonium supply. Isot Environ Health Stud 34:67–73

    Article  CAS  Google Scholar 

  7. Prasad P, Kalam S, Sharma NK, Podile AR, Das SNJFiA. (2022) Phosphate Solubilization and Plant Growth Promotion by Two Pantoea Strains Isolated from the Flower of Hedychium coronarium L. Front agron 990869:86

    Google Scholar 

  8. Feng Y, Shen D, Song W (2006) Rice endophyte Pantoea agglomerans YS19 promotes host plant growth and affects allocations of host photosynthates. J Appl Microbiol 100:938–945

    Article  CAS  PubMed  Google Scholar 

  9. Lim J-A, Lee DH, Kim B-Y, Heu S (2014) Draft genome sequence of Pantoea agglomerans R190, a producer of antibiotics against phytopathogens and foodborne pathogens. J Biotechnol 188:7–8

    Article  CAS  PubMed  Google Scholar 

  10. Mishra A, Chauhan PS, Chaudhry V, Tripathi M, Nautiyal CS (2011) Rhizosphere competent Pantoea agglomerans enhances maize (Zea mays) and chickpea (Cicer arietinum L.) growth, without altering the rhizosphere functional diversity. Anton Leeuw Int J G 100:405–413

    Article  Google Scholar 

  11. Remus-Emsermann MN, Kim EB, Marco ML, Tecon R, Leveau JH (2013) Draft genome sequence of the phyllosphere model bacterium Pantoea agglomerans 299R. Genome Announc 1:e00036-e113

    Article  PubMed  PubMed Central  Google Scholar 

  12. Houba V, Temminghoff E, Gaikhorst G, Van Vark W (2000) Soil analysis procedures using 0.01 M calcium chloride as extraction reagent. Commun Soil Sci Plant Anal 31:1299–1396

    Article  CAS  Google Scholar 

  13. Dahal RH, Chaudhary DK, Kim J (2017) Acinetobacter halotolerans sp. nov., a novel halotolerant, alkalitolerant, and hydrocarbon degrading bacterium, isolated from soil. Arch Microbiol 199:701–710

    Article  CAS  PubMed  Google Scholar 

  14. Banerjee S, Misra A, Chaudhury S, Dam B (2019) A Bacillus strain TCL isolated from Jharia coalmine with remarkable stress responses, chromium reduction capability and bioremediation potential. J Hazard Mater 367:215–223

    Article  CAS  PubMed  Google Scholar 

  15. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Kumar S, Nei M, Dudley J, Tamura K (2008) MEGA: a biologist-centric software for evolutionary analysis of DNA and protein sequences. Brief Bioinform 9:299–306

    Article  CAS  PubMed  Google Scholar 

  17. Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35:1547–1549

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Kumar S, Tamura K, Nei M (1994) MEGA: molecular evolutionary genetics analysis software for microcomputers. Bioinformatics 10:189–191

    Article  CAS  Google Scholar 

  19. Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. Retrieved 17 May 2018

  20. Andrews S, Krueger F, Segonds-Pichon A, Biggins L, Virk B, Dalle-Pezze P, Wingett S, Saadeh H, Ahlfors H (2015) Trim Galore

  21. Wick RR, Judd LM, Gorrie CL, Holt KE (2017) Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 13:e1005595

    Article  PubMed  PubMed Central  Google Scholar 

  22. Nikolenko SI, Korobeynikov AI, Alekseyev MA. BayesHammer: Bayesian clustering for error correction in single-cell sequencing. In: (ed). Springer, pp 1–11

  23. Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19:455–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Seemann T (2014) Prokka: rapid prokaryotic genome annotation. Bioinformatics 30:2068–2069

    Article  CAS  PubMed  Google Scholar 

  25. Grant JR, Stothard P (2008) The CGView Server: a comparative genomics tool for circular genomes. Nucleic Acids Res 36:W181–W184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Gurevich A, Saveliev V, Vyahhi N, Tesler G (2013) QUAST: quality assessment tool for genome assemblies. Bioinformatics 29:1072–1075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Guo Y, Zheng W, Rong X, Huang Y (2008) A multilocus phylogeny of the Streptomyces griseus 16S rRNA gene clade: use of multilocus sequence analysis for streptomycete systematics. Int J Syst Evol Microbiol 58:149–159

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  29. Meier-Kolthoff JP, Göker M (2019) TYGS is an automated high-throughput platform for state-of-the-art genome-based taxonomy. Nat Commun 10:1–10

    Article  CAS  Google Scholar 

  30. Eriksson A, Manica A (2014) The doubly conditioned frequency spectrum does not distinguish between ancient population structure and hybridization. Mol Biol Evol 31:1618–1621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Farris JS (1972) Estimating phylogenetic trees from distance matrices. Am Nat 106:645–668

    Article  Google Scholar 

  32. Richter M, Rosselló-Móra R, Oliver Glöckner F, Peplies J (2016) JSpeciesWS: a web server for prokaryotic species circumscription based on pairwise genome comparison. Bioinformatics 32:929–931

    Article  CAS  PubMed  Google Scholar 

  33. Kumar A, Kumar A, Thakur P, Patil S, Payal C, Kumar A, Sharma P (2012) Antibacterial activity of green tea (Camellia sinensis) extracts against various bacteria isolated from environmental sources. Recent Res Sci Technol 4:19–23

    Google Scholar 

  34. Priester JH, Horst AM, Van De Werfhorst LC, Saleta JL, Mertes LA, Holden PA (2007) Enhanced visualization of microbial biofilms by staining and environmental scanning electron microscopy. J Microbiol Methods 68:577–587

    Article  CAS  PubMed  Google Scholar 

  35. Suzuki Y, Kishigami T, Inoue K, Mizoguchi Y, Eto N, Takagi M, Abe S (1983) Bacillus thermoglucosidasius sp. nov., a new species of obligately thermophilic bacilli. Syst Appl Microbiol 4:487–495

    Article  CAS  PubMed  Google Scholar 

  36. Miskin A, Edberg SC (1978) Esculin hydrolysis reaction by Escherichia coli. J Clin Microbiol 7:251–254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Mukherjee T, Banik A, Mukhopadhyay SK (2020) Plant growth-promoting traits of a thermophilic strain of the Klebsiella group with its effect on rice plant growth. Curr Microbiol 77:2613–2622

    Article  CAS  PubMed  Google Scholar 

  38. Oskay M (2011) Effects of some environmental conditions on biomass and antimicrobial metabolite production by Streptomyces sp., KGG32. Int J Agric Biol 13:317–324

    CAS  Google Scholar 

  39. Lateef A, Oloke J, Gueguim-Kana E (2004) Antimicrobial resistance of bacterial strains isolated from orange juice products. Afr J Biotechnol 3:334–338

    Article  CAS  Google Scholar 

  40. Kunitsky C, Osterhout G, Sasser M (2006) Identification of microorganisms using fatty acid methyl ester (FAME) analysis and the MIDI sherlock microbial identification system. Encycl Rapid Microbiol Methods 3:1–18

    Google Scholar 

  41. Li C, Cano A, Acosta-Martinez V, Veum KS, Moore-Kucera J (2020) A comparison between fatty acid methyl ester profiling methods (PLFA and EL-FAME) as soil health indicators. Soil Sci Soc Am J 84:1153–1169

    Article  CAS  Google Scholar 

  42. Brady CL, Venter SN, Cleenwerck I, Engelbeen K, Vancanneyt M, Swings J, Coutinho TA (2009) Pantoea vagans sp. nov., Pantoea eucalypti sp. nov., Pantoea deleyi sp. nov. and Pantoea anthophila sp. nov. Int J Syst Evol Microbiol 59:2339–2345

    Article  CAS  PubMed  Google Scholar 

  43. Tanaka YK, Horie N, Mochida K, Yoshida Y, Okugawa E, Nanjo F (2015) Pantoea theicola sp. nov., isolated from black tea. Int J Syst Evol Microbiol 65:3313–3319

    Article  CAS  Google Scholar 

  44. Brady C, Cleenwerck I, Venter S, Coutinho T, De Vos P (2013) Taxonomic evaluation of the genus Enterobacter based on multilocus sequence analysis (MLSA): proposal to reclassify E. nimipressuralis and E. amnigenus into Lelliottia gen. nov. as Lelliottia nimipressuralis comb. nov. and Lelliottia amnigena comb. nov., respectively, E. gergoviae and E. pyrinus into Pluralibacter gen. nov. as Pluralibacter gergoviae comb. nov. and Pluralibacter pyrinus comb. nov., respectively, E. cowanii, E. radicincitans, E. oryzae and E. arachidis into Kosakonia gen. nov. as Kosakonia cowanii comb. nov., Kosakonia radicincitans comb. nov., Kosakonia oryzae comb. nov. and Kosakonia arachidis comb. nov., respectively, and E. turicensis, E. helveticus and E. pulveris into Cronobacter as Cronobacter zurichensis nom. nov., Cronobacter helveticus comb. nov. and Cronobacter pulveris comb. nov., respectively, and emended description of the genera Enterobacter and Cronobacter. Syst Appl Microbiol 36:309–319

    Article  PubMed  Google Scholar 

  45. Wei M, Wang P, Yang C, Gu L (2019) Molecular identification and phylogenetic relationships of clinical Nocardia isolates. Anton Leeuw Int J G 112:1755–1766

    Article  CAS  Google Scholar 

  46. Tambong JT, Xu R, Gerdis S, Daniels GC, Chabot D, Hubbard K, Harding MW (2021) Molecular analysis of bacterial isolates from necrotic wheat leaf lesions caused by Xanthomonas translucens, and description of three putative novel species, Sphingomonas albertensis sp. nov., Pseudomonas triticumensis sp. nov. and Pseudomonas foliumensis sp. nov. Front Microbiol 12:666689

    Article  PubMed  PubMed Central  Google Scholar 

  47. Pritchard L, Glover RH, Humphris S, Elphinstone JG, Toth IK (2016) Genomics and taxonomy in diagnostics for food security: soft-rotting enterobacterial plant pathogens. Anal Methods 8:12–24

    Article  Google Scholar 

  48. Stackebrandt E, Frederiksen W, Garrity GM, Grimont PA, Kämpfer P, Maiden MC, Nesme X, Rosselló-Mora R, Swings J, Trüper HG (2002) Report of the ad hoc committee for the re-evaluation of the species definition in bacteriology. Int J Syst Evol Microbiol 52:1043–1047

    CAS  PubMed  Google Scholar 

  49. Maiti PK, Mandal S (2021) Streptomyces himalayensis sp. nov. including Streptomyces himalayensis subsp. himalayensis subsp. nov. and Streptomyces himalayensis subsp. aureolus subsp. nov. isolated from Western Himalaya. Arch Microbiol 203:2325–2334

    Article  CAS  PubMed  Google Scholar 

  50. Fiedler G, Gieschler S, Kabisch J, Grimmler C, Brinks E, Wagner N, Hetzer B, Franz CM, Böhnlein C (2022) Pseudomonas rustica sp. nov., isolated from bulk tank raw milk at a German dairy farm. Int J Syst Evol Microbiol 72:1–11

    Article  Google Scholar 

  51. Brady CL, Cleenwerck I, Venter SN, Engelbeen K, De Vos P (2010) Emended description of the genus Pantoea, description of four species from human clinical samples, Pantoea septica sp. nov., Pantoea eucrina sp. nov., Pantoea brenneri sp. nov. and Pantoea conspicua sp. nov., and transfer of Pectobacterium cypripedii (Hori 1911) Brenner et al. 1973 emend. Hauben et al. 1998 to the genus as Pantoea cypripedii comb. nov. Int J Syst Evol Microbiol 60:2430–2440

    Article  CAS  PubMed  Google Scholar 

  52. Chen C, Xin K, Liu H, Cheng J, Shen X, Wang Y, Zhang L (2017) Pantoea alhagi, a novel endophytic bacterium with ability to improve growth and drought tolerance in wheat. Sci Rep 7:1–14

    Google Scholar 

  53. Brady CL, Goszczynska T, Venter SN, Cleenwerck I, De Vos P, Gitaitis RD, Coutinho TA (2011) Pantoea allii sp. nov., isolated from onion plants and seed. Int J Syst Evol Microbiol 61:932–937

    Article  CAS  PubMed  Google Scholar 

  54. UK C. 2014. Pantoea ananatis pv. ananatis ((Serrano, 1928) Mergaert et al., 1993), fruitlet rot of pineapple.[pest/pathogen].

  55. Gao J-l, Xue J, Yan H, Tong S, Khan MS, Wang L-w, Mao X-j, Zhang X, Sun J-g (2019) Pantoea endophytica sp. nov., novel endophytic bacteria isolated from maize planting in different geographic regions of northern China. Syst Appl Microbiol 42:488–494

    Article  PubMed  Google Scholar 

  56. Popp A, Cleenwerck I, Iversen C, De Vos P, Stephan R (2010) Pantoea gaviniae sp. nov. and Pantoea calida sp. nov., isolated from infant formula and an infant formula production environment. Int J Syst Evol Microbiol 60:2786–2792

    Article  CAS  PubMed  Google Scholar 

  57. Brady CL, Cleenwerck I, Van der Westhuizen L, Venter SN, Coutinho TA, De Vos P (2012) Pantoea rodasii sp. nov., Pantoea rwandensis sp. nov. and Pantoea wallisii sp. nov., isolated from Eucalyptus. Int J Syst Evol Microbiol 62:1457–1464

    Article  CAS  PubMed  Google Scholar 

  58. Pizzolante G, Durante M, Rizzo D, Di Salvo M, Tredici SM, Tufariello M, De Paolis A, Talà A, Mita G, Alifano P (2018) Characterization of two Pantoea strains isolated from extra-virgin olive oil. AMB Express 8:1–17

    Article  CAS  Google Scholar 

  59. Lefort V, Desper R, Gascuel O (2015) FastME 2.0: a comprehensive, accurate, and fast distance-based phylogeny inference program. Mol Biol Evol 32:2798–2800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Raju Biswas, Abhinaba Chakraborty, and Puja Mukherjee, are grateful to WB-DST, SERB, and CSIR for their fellowships. Prof. Manoranjan Chowdhury (North Bengal University, India) is acknowledged for his suggestions in determining the taxonomic nomenclature of the novel species. Funding from DST-PURSE is acknowledged for FE-SEM imaging and analysis.

Author information

Authors and Affiliations

Authors

Contributions

BD, RB, and AM designed the study. RB, and AM analyzed the data. RB, AM, SG, AC, PM, and BD wrote the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Bomba Dam.

Ethics declarations

Conflict of interest

The authors declare no conflict regarding financial or any academic interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 29568 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Biswas, R., Misra, A., Ghosh, S. et al. Pantoea tagorei sp. nov., a Rhizospheric Bacteria with Plant Growth-Promoting Activities. Indian J Microbiol (2023). https://doi.org/10.1007/s12088-023-01147-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12088-023-01147-9

Keywords

Navigation