Skip to content
1887

Abstract

A phosphate-solubilizing bacterial strain, designated C3, was isolated from the rhizosphere of sorghum. The taxonomic classification of this novel isolate was investigated by using a polyphasic approach. Cells of this strain were Gram-stain-negative, facultatively anaerobic and motile short rods with a polar flagellum. Phylogenetic analyses based on the 16S rRNA gene indicated that strain C3 showed high similarity (98.66%) to certain species, indicating that the isolate belongs to this genus. The genome of strain C3 was 5.05 Mb in size with a G+C content of 51.1 mol%. Whole-genome analysis revealed that the novel strain shared 21.60–27.10% digital DNA–DNA hybridization values and 78.35–83.87% average nucleotide identity with closely related species; both values below the accepted thresholds for defining a novel species. The predominant cellular fatty acids of strain C3 were C, summed feature 3 (C ω6c and/or C ω7c), summed feature 8 (C ω7c and/or C ω6c), summed feature 2 (C aldehyde and/or C 3OH and/or C iso I and/or an unidentified fatty acid of 10.9525 chain length) and C cyclo. Apart from the ability to solubilize phosphates, stain C3 exhibited other plant growth-promoting activities such as K, Ca and Si solubilization, and the production of indole-3-acetic acid (IAA) and siderophores. Several genes related to phosphate solubilization, siderophore biogenesis and IAA, cytokinin and gamma-aminobutyric acid production were identified in the C3 genome. Summarizing, based on phylogenetic, genomic, phenotypic and chemotaxonomic criteria, the isolate represents a novel species of the genus for which the name sp. nov. is proposed. The type strain is C3 (=CECT 31163=NCIMB 15596).

Funding
This study was supported by the:
  • Probelte S.A.U. (Award 40011)
    • Principal Award Recipient: AntonioSánchez-Amat
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
Loading

Article metrics loading...

/content/journal/ijsem/10.1099/ijsem.0.006764
2025-04-25
2026-01-16

Metrics

Loading full text...

Full text loading...

/deliver/fulltext/ijsem/75/4/ijsem006764.html?itemId=/content/journal/ijsem/10.1099/ijsem.0.006764&mimeType=html&fmt=ahah

References

  1. Adeolu M, Alnajar S, Naushad S, S Gupta R. Genome-based phylogeny and taxonomy of the “Enterobacteriales”: proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol 2016; 66:5575–5599 [View Article] [PubMed]
    [Google Scholar]
  2. Gavini F, Mergaert J, Beji A, Mielcarek C, Izard D et al. 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; 39:337–345 [View Article]
    [Google Scholar]
  3. Brady C, Venter S, Cleenwerck I, Vancanneyt M, Swings J et al. A FAFLP system for the improved identification of plant-pathogenic and plant-associated species of the genus Pantoea. Syst Appl Microbiol 2007; 30:413–417 [View Article] [PubMed]
    [Google Scholar]
  4. Tambong JT. Taxogenomics and systematics of the genus Pantoea. Front Microbiol 2019; 10: [View Article]
    [Google Scholar]
  5. Crosby KC, Rojas M, Sharma P, Johnson MA, Mazloom R et al. Genomic delineation and description of species and within-species lineages in the genus Pantoea. Front Microbiol 2023; 14:1254999 [View Article] [PubMed]
    [Google Scholar]
  6. Parte AC, Sardà Carbasse J, Meier-Kolthoff JP, Reimer LC, Göker M. List of Prokaryotic names with Standing in Nomenclature (LPSN) moves to the DSMZ. Int J Syst Evol Microbiol 2020; 70:5607–5612 [View Article] [PubMed]
    [Google Scholar]
  7. Walterson AM, Stavrinides J. Pantoea: insights into a highly versatile and diverse genus within the Enterobacteriaceae. FEMS Microbiol Rev 2015; 39:968–984 [View Article] [PubMed]
    [Google Scholar]
  8. Cruz AT, Cazacu AC, Allen CH. Pantoea agglomerans, a plant pathogen causing human disease. J Clin Microbiol 2007; 45:1989–1992 [View Article] [PubMed]
    [Google Scholar]
  9. Ruan XL, Qin X, Li M. Nosocomial bloodstream infection pathogen Pantoea dispersa: a case report and literature review. J Hosp Infect 2022; 127:77–82 [View Article] [PubMed]
    [Google Scholar]
  10. Rezzonico F, Stockwell VO, Tonolla M, Duffy B, Smits THM. Pantoea clinical isolates cannot be accurately assigned to species based on metabolic profiling. Transplant Infectious Dis 2012; 14:220–221 [View Article]
    [Google Scholar]
  11. Bomfeti CA, Souza-Paccola EA, Massola Júnior NS, Marriel IE, Meirelles WF et al. Localization of Pantoea ananatis inside lesions of maize white spot disease using transmission electron microscopy and molecular techniques. Trop plant pathol 2008; 33:63–66 [View Article]
    [Google Scholar]
  12. Abidin N, Ismail SI, Vadamalai G, Yusof MT, Hakiman M et al. Genetic diversity of Pantoea stewartii subspecies stewartii causing jackfruit-bronzing disease in Malaysia. PLoS One 2020; 15:e0234350 [View Article]
    [Google Scholar]
  13. Suleimanova A, Bulmakova D, Sokolnikova L, Egorova E, Itkina D et al. Phosphate solubilization and plant growth promotion by Pantoea brenneri soil isolates. Microorganisms 2023; 11:1136 [View Article]
    [Google Scholar]
  14. Luziatelli F, Ficca AG, Cardarelli M, Melini F, Cavalieri A et al. Genome sequencing of Pantoea agglomerans C1 provides Insights into molecular and genetic mechanisms of plant growth-promotion and tolerance to heavy metals. Microorganisms 2020; 8:153
    [Google Scholar]
  15. Castagno LN, Estrella MJ, Sannazzaro AI, Grassano AE, Ruiz OA. 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 2011; 110:1151–1165
    [Google Scholar]
  16. Wdowiak-Wróbel S, Kalita M, Palusińska-Szysz M, Marek-Kozaczuk M, Sokołowski W et al. Pantoea trifolii sp. nov., a novel bacterium isolated from Trifolium rubens root nodules. Sci Rep 2024; 14:2698 [View Article] [PubMed]
    [Google Scholar]
  17. Chauhan H, Bagyaraj DJ, Selvakumar G, Sundaram SP. Novel plant growth promoting rhizobacteria—prospects and potential. Appl Soil Ecol 2015; 95:38–53 [View Article]
    [Google Scholar]
  18. Ramakrishna W, Yadav R, Li K. Plant growth promoting bacteria in agriculture: two sides of a coin. Appl Soil Ecol 2019; 138:10–18 [View Article]
    [Google Scholar]
  19. Chapke RR, Tonapi VA. Adoption and socio-economic benefits of improved post-rainy sorghum production technology. Agric Res 2019; 8:270–278 [View Article]
    [Google Scholar]
  20. Carlson R, Tugizimana F, Steenkamp PA, Dubery IA, Hassen AI et al. Rhizobacteria-induced systemic tolerance against drought stress in Sorghum bicolor (L.) Moench. Microbiol Res 2020; 232:126388 [View Article] [PubMed]
    [Google Scholar]
  21. Nautiyal CS. An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 1999; 170:265–270 [View Article] [PubMed]
    [Google Scholar]
  22. Hongoh Y, Yuzawa H, Ohkuma M, Kudo T. Evaluation of primers and PCR conditions for the analysis of 16S rRNA genes from a natural environment. FEMS Microbiol Lett 2003; 221:299–304 [View Article] [PubMed]
    [Google Scholar]
  23. Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y et al. Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 2017; 67:1613–1617 [View Article] [PubMed]
    [Google Scholar]
  24. Yarza P, Yilmaz P, Pruesse E, Glöckner FO, Ludwig W et al. Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences. Nat Rev Microbiol 2014; 12:635–645 [View Article] [PubMed]
    [Google Scholar]
  25. Thompson JD, Higgins DG, Gibson TJ. 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; 22:4673–4680 [View Article] [PubMed]
    [Google Scholar]
  26. Tamura K, Stecher G, Kumar S. MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Mol Biol Evol 2021; 38:3022–3027 [View Article] [PubMed]
    [Google Scholar]
  27. Saitou N, Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 1987; 4:406–425 [View Article] [PubMed]
    [Google Scholar]
  28. Felsenstein J. Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 1981; 17:368–376 [View Article] [PubMed]
    [Google Scholar]
  29. Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 1985; 39:783–791 [View Article] [PubMed]
    [Google Scholar]
  30. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 1980; 16:111–120 [View Article] [PubMed]
    [Google Scholar]
  31. Koren S, Walenz BP, Berlin K, Miller JR, Bergman NH et al. Canu: scalable and accurate long-read assembly via adaptive. Genome Res 2017; 27:722–736 [View Article]
    [Google Scholar]
  32. Loman NJ, Quick J, Simpson JT. A complete bacterial genome assembled de novo using only nanopore sequencing data. Nat Methods 2015; 12:733–735 [View Article] [PubMed]
    [Google Scholar]
  33. Wick RR, Judd LM, Gorrie CL, Holt KE. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput Biol 2017; 13:e1005595 [View Article] [PubMed]
    [Google Scholar]
  34. Seemann T. Prokka: rapid prokaryotic genome annotation. Bioinform 2014; 30:2068–2069 [View Article] [PubMed]
    [Google Scholar]
  35. Seemann T, Booth T. Barrnap: basic rapid ribosomal RNA predictor. GitHub repository 2018
    [Google Scholar]
  36. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997; 25:955–964 [View Article] [PubMed]
    [Google Scholar]
  37. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25:1043–1055 [View Article] [PubMed]
    [Google Scholar]
  38. Hara Y, Kadotani N, Izui H, Katashkina JI, Kuvaeva TM et al. The complete genome sequence of Pantoea ananatis AJ13355, an organism with great biotechnological potential. Appl Microbiol Biotechnol 2012; 93:331–341 [View Article] [PubMed]
    [Google Scholar]
  39. Smits THM, Rezzonico F, Pelludat C, Goesmann A, Frey JE et al. Genomic and phenotypic characterization of a nonpigmented variant of Pantoea vagans biocontrol strain C9-1 lacking the 530-kb megaplasmid pPag3. FEMS Microbiol Lett 2010; 308:48–54 [View Article] [PubMed]
    [Google Scholar]
  40. Zeng Q, Shi G, Nong Z, Ye X, Hu C. Complete genome sequence of Pantoea ananatis strain NN08200, an endophytic bacterium isolated from sugarcane. Curr Microbiol 2020; 77:1864–1870 [View Article] [PubMed]
    [Google Scholar]
  41. Brady CL, Cleenwerck I, Venter SN, Engelbeen K, Vos P et al. 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 1911; 60:2430–2440 [View Article]
    [Google Scholar]
  42. Yoon S-H, Ha S-M, Lim J, Kwon S, Chun J. A large-scale evaluation of algorithms to calculate average nucleotide identity. Antonie van Leeuwenhoek 2017; 110:1281–1286 [View Article] [PubMed]
    [Google Scholar]
  43. Meier-Kolthoff JP, Auch AF, Klenk H-P, Göker M. Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 2013; 14:60 [View Article] [PubMed]
    [Google Scholar]
  44. Meier-Kolthoff JP, Carbasse JS, Peinado-Olarte RL, Göker M. TYGS and LPSN: a database tandem for fast and reliable genome-based classification and nomenclature of prokaryotes. Nucleic Acids Res 2022; 50:D801–D807 [View Article] [PubMed]
    [Google Scholar]
  45. Riesco R, Trujillo ME. Update on the proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 2024; 74:006300 [View Article] [PubMed]
    [Google Scholar]
  46. Boxberger M, Ben Khedher M, Magnien S, Cassir N, La Scola B. Draft genome and description of Microvirga mediterraneensis strain Marseille-Q2068T sp. nov., a new bacterium isolated from human healthy skin. New Microbes New Infect 2021; 40:100839 [View Article] [PubMed]
    [Google Scholar]
  47. Göker M, Moore ERB, Oren A, Trujillo ME. Status of the SeqCode in the international journal of systematic and evolutionary microbiology. Int J Syst Evol Microbiol 2023; 72: [View Article]
    [Google Scholar]
  48. Aziz RK, Devoid S, Disz T, Edwards RA, Henry CS et al. SEED servers: high-performance access to the SEED genomes, annotations, and metabolic models. PLoS One 2012; 7:e48053 [View Article] [PubMed]
    [Google Scholar]
  49. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ et al. The SEED and the rapid annotation of microbial genomes using subsystems technology (RAST). Nucleic Acids Res 2014; 42:D206–14 [View Article] [PubMed]
    [Google Scholar]
  50. Blin K, Shaw S, Augustijn HE, Reitz ZL, Biermann F et al. antiSMASH 7.0: new and improved predictions for detection, regulation, chemical structures and visualisation. Nucleic Acids Res 2023; 51:W46–W50 [View Article] [PubMed]
    [Google Scholar]
  51. Rodríguez H, Fraga R, Gonzalez T, Bashan Y. Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant Soil 2006; 287:15–21 [View Article]
    [Google Scholar]
  52. Ahmed E, Holmström SJM. Siderophores in environmental research: roles and applications. Microb Biotechnol 2014; 7:196–208
    [Google Scholar]
  53. Nascimento FX, Hernandez AG, Glick BR, Rossi MJ. The extreme plant-growth-promoting properties of pantoea phytobeneficialis MSR2 revealed by functional and genomic analysis. Environ Microbiol 2020; 22:1341–1355
    [Google Scholar]
  54. Grammbitter GLC, Schmalhofer M, Karimi K, Shi YM, Schöner TA et al. An uncommon type II PKS catalyzes biosynthesis of aryl polyene pigments. J Am Chem Soc 2019; 141:16615–16623
    [Google Scholar]
  55. Sedkova N, Tao L, Rouvière Pierre E, Cheng Q. Diversity of carotenoid synthesis gene clusters from environmental Enterobacteriaceae strains. Appl Environ Microbiol 2005; 71:8141–8146
    [Google Scholar]
  56. Ciche TA, Blackburn M, Carney JR, Ensign JC. Photobactin: a catechol siderophore produced by Photorhabdus luminescens, an entomopathogen mutually associated with Heterorhabditis bacteriophora NC1 nematodes. Appl Environ Microbiol 2003; 69:4706–4713 [View Article] [PubMed]
    [Google Scholar]
  57. Coico R. Gram staining. Curr Protoc Microbiol 2006; 00: [View Article]
    [Google Scholar]
  58. Parmar P, Sindhu SS. The novel and efficient method for isolating potassium solubilizing bacteria from rhizosphere soil. Geomicrobiol J 2019; 36:130–136 [View Article]
    [Google Scholar]
  59. Rana G, Mandal T, Mandal NK, Sakha D, Meikap BC. Calcite solubilization by bacteria: a novel method of environment pollution control. Geomicrobiol J 2015; 32:846–852 [View Article]
    [Google Scholar]
  60. Bist V, Niranjan A, Ranjan M, Lehri A, Seem K et al. Silicon-solubilizing media and its implication for characterization of bacteria to mitigate biotic stress. Front Plant Sci 2020; 11:28 [View Article] [PubMed]
    [Google Scholar]
  61. Louden BC, Haarmann D, Lynne AM. Use of blue agar CAS assay for siderophore detection. J Microbiol Biol Educ 2011; 12:51–53 [View Article] [PubMed]
    [Google Scholar]
  62. Naik PR, Sahoo N, Goswami D, Ayyadurai N, Sakthivel N. Genetic and functional diversity among fluorescent pseudomonads isolated from the rhizosphere of banana. Microb Ecol 2008; 56:492–504 [View Article] [PubMed]
    [Google Scholar]
  63. Kasana RC, Salwan R, Dhar H, Dutt S, Gulati A. A rapid and easy method for the detection of microbial cellulases on agar plates using gram’s iodine. Curr Microbiol 2008; 57:503–507 [View Article] [PubMed]
    [Google Scholar]
  64. Herrera-Quiterio A, Toledo-Hernández E, Aguirre-Noyola JL, Romero Y, Ramos J et al. Antagonic and plant growth-promoting effects of bacteria isolated from mine tailings at El Fraile, Mexico. Rev Argent Microbiol 2020; 52:231–239 [View Article] [PubMed]
    [Google Scholar]
  65. Chen C, Xin K, Liu H, Cheng J, Shen X et al. Pantoea alhagi, a novel endophytic bacterium with ability to improve growth and drought tolerance in wheat. Sci Rep 2017; 7:41564 [View Article] [PubMed]
    [Google Scholar]
  66. Sasser M. Identification of bacteria by gas chromatography of cellular fatty acids. In MIDI Technical Note 1990
    [Google Scholar]
  67. MIDI Sherlock microbial identification system operating manual, version 6.1. Inc Newark, DE: MIDI; 2008
  68. Biswas R, Misra A, Ghosh S, Chakraborty A, Mukherjee P et al. Pantoea tagorei sp. nov., a rhizospheric bacteria with plant growth-promoting activities. Indian J Microbiol 2024; 64:937–949 [View Article] [PubMed]
    [Google Scholar]
/content/journal/ijsem/10.1099/ijsem.0.006764
Loading
/content/journal/ijsem/10.1099/ijsem.0.006764
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An error occurred
Approval was partially successful, following selected items could not be processed due to error