Multifarious plant growth promoting ability of Pseudomonas extremorientalis RPB22 enhances chickpea (Cicer arietinum) growth

SAMADHAN YUVRAJ  BAGUL; RITU RAJ  PATEL; RITU  VISHWAKARMA; HILLOL  CHAKDAR; PANDIYAN  K; KUMAR M; MAGESHWARAN  VELLAICHAMY; RAGHUNANDAN  B L; ALOKK KUMAR  SRIVASTAVA

doi:10.56093/ijas.v96i1.154342

Authors

SAMADHAN YUVRAJ BAGUL ICAR-Directorate of Medicinal Aromatic Plant Research, Boriavi, Anand, Gujarat, India
RITU RAJ PATEL Institute of Medical Sciences, Banaras Hindu University, Varanasi, Uttar Pradesh, India
RITU VISHWAKARMA ICAR-National Bureau of Agriculturally Important Microorganisms, Mau, Uttar Pradesh, India
HILLOL CHAKDAR ICAR-National Bureau of Agriculturally Important Microorganisms, Mau, Uttar Pradesh, India
Pandian K ICAR-Directorate of Medicinal Aromatic Plant Research, Boriavi, Anand, Gujarat, India
KUMAR M ICAR-National Bureau of Agriculturally Important Microorganisms, Mau, Uttar Pradesh, India
MAGESHWARAN VELLAICHAMY ICAR-National Bureau of Agriculturally Important Microorganisms, Mau, Uttar Pradesh, India
RAGHUNANDAN B L College of Natural Farming, Natural Farming Science University, Halol, Panchmahal, Gujarat, India
ALOKK KUMAR SRIVASTAVA ICAR-National Bureau of Agriculturally Important Microorganisms, Mau, Uttar Pradesh, India

https://doi.org/10.56093/ijas.v96i1.154342

Keywords:

Hot spring, HPLC, Organic acid, Phosphate, Plant growth promotion, Thermo-tolerance

Abstract

The present study was carried out during 2020–2021 at ICAR-National Bureau of Agriculturally Important Microorganisms, Mau, Uttar Pradesh to assess the plant growth-promoting potential of a bacterial isolate obtained from the hot water spring at Tattapani, Chhattisgarh. The hot spring exhibited a temperature of 80°C and a pH of 7.5. Molecular characterization identified the isolate as Pseudomonas extremorientalis strain RPB22. This strain showed tolerance to salinity up to 3% NaCl and temperature of 50°C. Strain RPB22 efficiently solubilized inorganic tri-calcium phosphate (333 ± 9 µg/mL) and potassium (10.5 mg/L). High-Performance Liquid Chromatography (HPLC) analysis revealed the production of several organic acids, predominantly malic acid, followed by oxalic acid. Seed treatment of chickpea with strain RPB22 led to a 2.75-fold and 2.17-fold increase in fresh root and shoot dry weight, respectively, while root volume increased 1.8-fold compared to the untreated control. These findings highlight the potential of P. extremorientalis RPB22 as a thermo-tolerant, multifaceted plant growth-promoting bacterium suitable for biofertilizer development in arid and semi-arid environments exposed to high temperatures.

Downloads

Download data is not yet available.

References

Ahmad F, Ahmad I and Khan M S. 2005. Indole acetic acid production by the indigenous isolates of Azotobacter and fluorescent Pseudomonas in the presence and absence of tryptophan. Turkish Journal of Biology 29(1): 29–34.

Ahmad M, Imtiaz M, Nawaz M S, Mubin F, Sarwar Y, Hayat M, Asif M, Naqvi R Z, Ahmad M and Imran A. 2023. Thermotolerant PGPR consortium B3P modulates physio-biochemical and molecular machinery for enhanced heat tolerance in maize during early vegetative growth. Annals of Microbiology 73: 34. https://doi.org/10.1186/s13213-023-01736-5 DOI: https://doi.org/10.1186/s13213-023-01736-5

Ahemed M and Kibret M. 2014. Mechanisms and applications of plant growth promoting rhizobacteria: Current perspective. Journal of King Saud University-Science 26: 1–20. https://doi. org/10.1016/j.jksus.2013.05.001 DOI: https://doi.org/10.1016/j.jksus.2013.05.001

Alonazi M A, Alwathnani H A, AL-Barakah F N I and Alotaibi F. 2025. Native plant growth-promoting rhizobacteria containing ACC Deaminase promote plant growth and alleviate salinity and heat stress in maize (Zea mays L.) plants in Saudi Arabia. Plants 14(7): 1107. https://doi.org/10.3390/plants14071107 DOI: https://doi.org/10.3390/plants14071107

Amaresan N, Kumar K, Sureshbabu K and Madhuri K. 2014. Plant growth-promoting potential of bacteria isolated from active volcano sites of Barren Island, India. Letters in Applied Microbiology 58(2): 130–37. Doi: 10.1111/lam.12165 DOI: https://doi.org/10.1111/lam.12165

Badhai J, Ghosh T S and Das S K. 2015. Taxonomic and functional characteristics of microbial communities and their correlation with physicochemical properties of four geothermal springs in Odisha, India. Frontiers in Microbiology 6: 1166. https://doi.org/10.3389/fmicb.2015.01166 DOI: https://doi.org/10.3389/fmicb.2015.01166

Banerjee S, Barjas C B, Tapia J, Fabi J P, Banerjee D S, Barjas G C, Tapia J, Fabi J P, Delattre C and Banerjee A. 2024. Characterization of Chilean hot spring-origin Staphylococcus spp. BSP3 produced exopolysaccharide as biological additive. Natural Products and Biology 14: 15. https://doi.org/10.1007/ s13659-024-00436-0 DOI: https://doi.org/10.1007/s13659-024-00436-0

Brick J M, Bostock R M and Silverstone S E. 1991. Rapid in situ assay for indole acetic acid production by bacteria immobilized on nitrocellulose membrane. Applied Environmental Microbiology 57: 535–38. 10.1128/aem.57.2.535-538.1991 DOI: https://doi.org/10.1128/aem.57.2.535-538.1991

Castelan-Sanchez H G, Fernandez Dodero J V, Rojas-Vargas J, Martínez-Ocampo F, Hurtado-Ramirez J M, Ríos-Vazquez D I, SAnchez-Alonso P, Vazquez-Cruz C and Rojas-Ruiz N E. 2025. Thermophilic Pseudomonas aeruginosa strain Ch39 isolated from Chignahuapan hot springs in Puebla, Mexico. Letters in Applied Microbiology 78: 4. https://doi.org/10.1093/lambio/ovaf059 DOI: https://doi.org/10.1093/lambio/ovaf059

Fiske C H and Subbarow Y. 1925. The colourimetric determination of phosphorus. Journal of Biology and Chemistry 66: 375–400. DOI: https://doi.org/10.1016/S0021-9258(18)84756-1

Ghati A, Sarkar K and Paul G. 2013. Isolation, characterization and molecular identification of esterolytic thermophilic bacteria from an Indian hot spring. Current Research in Microbiology and Biotechnology 1(4): 196–202.

Gontia-Mishra I, Sapre S and Tiwari S. 2017. Zinc solubilising bacteria from the rhizosphere of rice as prospective modulator of zinc biofortification in rice. Rhizosphere 3: 185–90. https:// doi.org/10.1016/j.rhisph.2017.04.013 DOI: https://doi.org/10.1016/j.rhisph.2017.04.013

Gopalakrishnan S, Vadlamudi S, Samineni S and Kumar S S. 2016. Plant growth-promotion and biofortification of chickpea and pigeonpea through inoculation of biocontrol potential bacteria, isolated from organic soils. Springer Plus 5: 1882. Doi 10.1186/s40064-016-3590-6 DOI: https://doi.org/10.1186/s40064-016-3590-6

Jackson M L. 1958. Soil Chemical Analysis. pp. 498. Prentice-Hall Inc., Englewood Cliffs, New Jersey.

Jha U C, Nath C P, Paul P J, Nayyar H, Kumar N, Dixit G P, Sen S, Kumar Y and Prasad P V V. 2025. Decoding the heat stress resilience in Chickpea (Cicer arietinum L.): Multi-trait analysis for genotypic adaptation. Scientific Report 15(1): 25055. Doi: 10.1038/s41598-025-07573-7. DOI: https://doi.org/10.1038/s41598-025-07573-7

Kumar M, Yadav A N, Tiwari R, Prasanna R and Saxena A K. 2014. Deciphering the diversity of culturable thermotolerant bacteria from Manikaran hot springs. Annals of Microbiology 64: 741–51. doi.org/10.1007/s13213-013-0709-7 DOI: https://doi.org/10.1007/s13213-013-0709-7

Mirete S, Morgante V and Gonzalez-Pastor J E. 2016. Functional metagenomics of extreme environments. Current Opinion in Biotechnology 38: 143–49. Doi: 10.1016/j.copbio.2016.01.017 DOI: https://doi.org/10.1016/j.copbio.2016.01.017

Mongra A C. 2012. Distribution pattern of cyanobacteria in hot water springs of Tattapani, Himachal Pradesh, India. Journal of Academia and Industrial Research 1: 363–70.

Mukherjee T, Banik A and Mukhopadhyay S K. 2020. Plant growth promoting traits of a thermophilic strain of the Klebsiella group with its effect on rice plant growth. Current Microbiology 77(10): 2613–22. Doi: 10.1007/s00284-020-02032-0 DOI: https://doi.org/10.1007/s00284-020-02032-0

Munoz-Torres P, Marquez S L, Sepulveda-Chavera G, Cardenas-Ninasivincha S, Arismendi-Macuer M, Huanca-Mamani W, Aguilar Y, Quezada A and Bugueno F. 2023. Isolation and identification of bacteria from three geothermal sites of the Atacama Desert and their plant-beneficial characteristics. Microorganisms 11: 2635. DOI: https://doi.org/10.3390/microorganisms11112635

Nshimiyimana J B, Khadka S, Mwizerwa M E, Akimana N, Adhikari S and Nsabimana A. 2018. Thermophiles: Isolation, characterization and screening for enzymatic activity. Bioscience Discovery 9(3): 430–37.

Oteino N, Lally R D, Kiwanuka S, Lloyd A, Ryan D, Germaine K J and Dowling D N. 2015. Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Frontiers in Microbiology 6: 745. DOI: https://doi.org/10.3389/fmicb.2015.00745

Pandey A, Dhakar K, Sharma A, Priti P, Sati P and Kumar B. 2015. Thermophilic bacteria that tolerate a wide temperature and pH range colonize the Soldhar (95ºC) and Ringigad (80ºC) hot springs of Uttarakhand, India. Annals of Microbiology 65(2): 809–16. https://doi.org/10.1007/s13213-014-0921-0 DOI: https://doi.org/10.1007/s13213-014-0921-0

Patel J K and Archana G. 2017. Diverse culturable diazotrophic endophytic bacteria from poaceae plants show cross-colonization and plant growth promotion in wheat. Plant and Soil 417(1–2): 99–116. DOI: https://doi.org/10.1007/s11104-017-3244-7

Perez E, Sulbaran M, Ball M M and Yarzabal L A. 2007. Isolation and characterization of mineral phosphate-solubilizing bacteria naturally colonizing a limonitic crust in the south-eastern Venezuelan region. Soil Biology and Biochemistry 39(11): 2905–14. https://doi.org/10.1016/j.soilbio.2007.06.013 DOI: https://doi.org/10.1016/j.soilbio.2007.06.017

Pikovskaya R I. 1948. Mobilisation of phosphorus in soil in connection with the vital activity of some microbial species. Microbiologia 17: 362–70.

Purcell U, Sompong L C, Yim T G, Barraclough Y and Peerapornpisal S B. 2007. Pointing the effects of temperature, pH and sulphide on the community structure of hyperthermophilic streamers in hot springs of northern Thailand. FEMS Microbiology and Ecology 60: 456–66. Doi: 10.1111/j.1574-6941.2007.00302.x DOI: https://doi.org/10.1111/j.1574-6941.2007.00302.x

Rajawat M V, Singh S, Saxena A and Prasanna A. 2016. A modified plate assay for rapid screening of potassium-solubilising bacteria. Pedosphere 26(5): 768–73. https://doi.org/10.1016/ S1002-0160(15)60080 DOI: https://doi.org/10.1016/S1002-0160(15)60080-7

Sayeh R, Birrien J L, Alain K, Barbier G, Hamdi M and Prieur D. 2010. Microbial diversity in Tunisian geothermal springs as detected by molecular and culture-based approaches. Extremophiles 14(6): 501–14. Doi: 10.1007/s00792-010-0327-2 DOI: https://doi.org/10.1007/s00792-010-0327-2

Saxena R, Dhakan D B, Mittal P, Waiker P, Chowdhury A, Ghatak A and Sharma V K. 2017. Metagenomic analysis of hot springs in central India reveals hydrocarbon degrading thermophiles and pathways essential for survival in extreme environments. Frontiers in Microbiology 5(7): 2123. https://doi.org/10.3389/ fmicb.2016.02123 DOI: https://doi.org/10.3389/fmicb.2016.02123

Schwyn B and Neilands J B. 1987. Universal chemical assay for the detection and determination of siderophores. Analytical Biochemistry 160(1): 47–56. Doi: 10.1016/0003-2697(87)90612-9 DOI: https://doi.org/10.1016/0003-2697(87)90612-9

Sharma A, Kohli P, Singh Y, Schumann P and Lal R. 2016. Fictibacillus halophilus sp. nov., from a microbial mat of a hot spring atop the Himalayan Range. International Journal of Systematic and Evolutionary Microbiology 66(6): 2409–16. Doi: 10.1099/ijsem.0.001051 DOI: https://doi.org/10.1099/ijsem.0.001051

Sood G, Prakash V and Arora S. 2024. Diversity of multi trait plant growth-promoting culturable bacteria from natural geothermal springs. Geomicrobiology Journal 41(5): 543–51. Doi: 10.1080/01490451.2024.2335941 DOI: https://doi.org/10.1080/01490451.2024.2335941

Soy S, Nigam V N and Sharma S R. 2019. Cellulolytic, amylolytic and xylanolytic potential of thermophilic isolates of Surajkund hot spring. Journal of Bioscience 44: 124. Doi: 10.1007/ s12038-019-9938-7 DOI: https://doi.org/10.1007/s12038-019-9938-7

Sridevi M and Mallaiah K V. 2007. Bioproduction of indole acetic acid by Rhizobium strains isolated from root nodules of green manure crop, Sesbania sesban (L.) Merr. Iranian Journal of Biotechnology 5(3): 178–82.

Thakur R and Yadav S. 2023. Thermotolerant and halotolerant Streptomyces spp. isolated from Ajuga parviflora having biocontrol activity against Pseudomonas syringae and Xanthomonas campestris acts as a sustainable bioadditive in growth promotion of Cicer arietinum. Physiological and Molecular Plant Pathology 127: 2023. https://doi.org/10.1016/j. pmpp.2023.102059 DOI: https://doi.org/10.1016/j.pmpp.2023.102059

Tanimoto E. 2005. Regulation of root growth by plant hormones–Roles for auxin and gibberellin. Critical Review in Plant Science 24: 249–65. Doi: 10.1080/07352680500196108 DOI: https://doi.org/10.1080/07352680500196108

Verma J P, Jaiswal D K, Krishna R, Prakash R, Yadav J and Singh V. 2018. Characterization and screening of thermophilic bacillus strains for developing plant growth promoting consortium from hot spring of Leh and Ladakh region of India. Frontiers in Microbiology 9: 1293. https://doi.org/10.3389/ fmicb.2018.01293 DOI: https://doi.org/10.3389/fmicb.2018.01293

Verma J, Sourirajan A and Dev K. 2022. Bacterial diversity in 110 thermal hot springs of Indian Himalayan Region (IHR). 3 Biotech 12(9): 238. Doi: 10.1007/s13205-022-03270-8 DOI: https://doi.org/10.1007/s13205-022-03270-8

Yadav A N, Verma P, Kumar M, Pal K K, Dey R, Gupta A, Padaria J C, Gujar G T, Kumar S, Suman A, Prasanna R and Saxena A K. 2015. Diversity and phylogenetic profiling of niche-specific Bacilli from extreme environments of India. Annals of Microbiology 65: 611–29. https://doi.org/10.1007/ s13213-014-0897-9 DOI: https://doi.org/10.1007/s13213-014-0897-9

Yoon S H, Ha S M, Kwon S, Lim J, Kim Y, Seo H and Chun J. 2017. Introducing EzBioCloud: A taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. International Journal of Systematics and Evolutionary Microbiology 67(5): 1613. https://doi. org/ 10.1099/ ijsem.0. 001755 DOI: https://doi.org/10.1099/ijsem.0.001755

Vyas P and Gulati A. 2009. Organic acid production in vitro and plant growth promotion in maize under controlled environment by phosphate-solubilizing fluorescent Pseudomonas. BMC Microbiology 9: 174. https://doi.org/10.1186/1471-2180-9-174 DOI: https://doi.org/10.1186/1471-2180-9-174

Zhang J, Tang S K, Zhang Y Q, Yu L Y, Klenk H P and Li W J. 2010. Laceyella tengchongensis sp. nov., a thermophile isolated from soil of a volcano. International Journal of Systematics and Evolutionary Microbiology 60: 2226–30. Doi: 10.1099/ ijs.0.011767-0 DOI: https://doi.org/10.1099/ijs.0.011767-0