Isolation and identification of salt tolerant-plant growth promoting bacteria from the rhizosphere of halophyte plants

Document Type : Complete scientific research article

Authors

1 PhD student, Soil Science Department, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran.

2 Associate Professor, Soil Science Department, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran.

3 Assistant Professor, Soil Science Department, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran

4 79 / 5,000 Translation results Translation result Associate Professor, Soil Science Department, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran.

5 Assistant Professor, Tabaristan Agricultural Genetics and Biotechnology Research Institute, Sari University of Agricultural Sciences and Natural Resources, Sari, Iran.

Abstract

Isolation and identification of salt tolerant-plant growth promoting bacteria from the rhizosphere of halophyte plants
Background and purpose: Salinity is a serious problem and one of the main factors in reducing agricultural productivity worldwide. The use of microorganisms to improve plant growth in low quality soil is a potential solution to address this problem. The salinity resistant microbiome improves the health of the salinity affected soils, maintains ecological functions and enhances plant growth. Salt tolerant plant growth promoting rhizobacteria (ST-PGPR) are able to adjust the salinity stress adverse conditions for their symbiotic plants through several mechanisms. This study aimed to isolation, identification and investigation the characteristics of salt tolerant-plant growth promoting rhizobacteria from the rhizosphere of halophyte plants.
Materials and methods: Salinity tolerant plant growth promoting bacteria were isolated from the rhizosphere of native halophyte plants collected from the north of Iran. Bacterial isolates were selected according to their ability to growth in 2 M sodium chloride and traits of the motility, inorganic phosphate solubilization ability in PKV-Agar medium using phosphate solubilization index calculation, and siderophore production capacity in CAS-agar medium by calculating of its production index. Then, the top 10 isolates were selected and the ability of nitrogen fixation in Burk's medium, potassium dissolution in Aleksandrov's medium by using potassium solubilization index, as well as, the production of intrinsic IAA and the tryptophan-dependent IAA were investigated. Finally, molecular identification of selected bacterial isolates was performed based on 16S rDNA gene sequencing.
Findings: Four genera of Bacillus, Klebsiella, Proteus and Halomonas were identified after 16S rDNA gene sequencing. All isolates were motile. The most of isolates belonged to the genus Bacillus. Species belonging to Klebsiella and Halomonas genera had the highest salt tolerance. Klebsiella genus showed phosphorus and potassium solubilizing ability more than other isolates. The highest amount of siderophore production was observed in the isolate belonging to Proteus genus. All isolates were able to fix nitrogen. Among the studied isolates, Bacillus isolates had the highest rate of intrinsic IAA, and the tryptophan-dependent IAA production in B. licheniformis was higher than other isolates.
Conclusion: Isolation of wide range of salt-tolerant bacteria with favorable characteristics from the rhizosphere of halophyte plants indicates the microbial richness potential of this area, which provides the possibility of finding useful microorganisms that promote plant growth and reduce the adverse effects of stress in plants.
Keywords: Plant growth promoting bacteria, Salinity stress, Halophyte plants, Indole acetic acid

Keywords

Main Subjects

References

1.Kapadia, C., Patel, N., Rana, A., Vaidya, H., Alfarraj, S., Ansari, M. J., Gafur, A., Poczai, P. & Sayyed, R. Z. (2022). Evaluation of plant growth-promoting and salinity ameliorating potential of halophilic bacteria isolated from saline soil. Frontiers in Plant Science, 13, 1-14. doi:10.3389/fpls.2022.946217.
2.Santoyo, G., Urtis-Flores, C. A., Loeza-Lara, P. D., Orozco-Mosqueda, M. D. C., & Glick, B. R. (2021). Rhizosphere colonization determinants by plant growth-promoting rhizobacteria (PGPR). Biology, 10 (6), 1-18. doi:10.3390/ biology10060475.
3.Egamberdieva, D., Wirth, S., Bellingrath-Kimura, S. D., Mishra, J., & Arora, N. K. (2019). Salt-tolerant plant growth promoting rhizobacteria for enhancing crop productivity of saline soils. Frontiers in Microbiology, 10, 1-18. doi:10.3389/fmicb.2019.02791.
4.Castiglione, S., Oliva, G., Vigliotta, G., Novello, G., Gamalero, E., Lingua, G., Cicatelli, A., & Guarino, F. (2021). Effects of compost amendment on glycophyte and halophyte crops grown on saline soils: Isolation and characterization of rhizobacteria with plant growth promoting features and high salt resistance. Applied Sciences, 11 (5), 1-15. doi:10.3390/app11052125.
5.Schirawski, J., & Perlin, M. H. (2018). Plant–microbe interaction 2017-the good, the bad and the diverse. International Journal of Molecular Sciences, 19 (5), 1-6. doi:10.3390/ijms 19051374.
6.Kearl, J., McNary, C., Lowman, J. S., Mei, C., Aanderud, Z. T., Smith, S. T., West, E., Colton, M., Hamson., & Nielsen, B. L. (2019). Salt-tolerant halophyte rhizosphere bacteria stimulate growth of alfalfa in salty soil. Frontiers in Microbiology, 10, 1-11. doi:10.3389/ fmicb.2019.01849.
7.Palacio-Rodríguez, R., Coria-Arellano, J. L., López-Bucio, J., Sánchez-Salas, J., Muro-Pérez, G., Castañeda-Gaytán, G., & Sáenz-Mata, J. (2017). Halophilic rhizobacteria from Distichlis spicata promote growth and improve salt tolerance in heterologous plant hosts. Symbiosis, 73, 179-189. doi:10.1007/ s13199-017-0481-8.
8.Castellano-Hinojosa, A., & Bedmar, E. J. (2017). Methods for evaluating plant growth-promoting rhizobacteria traits.
P 255-274, In: H.B. Singh, B. K. Sarma, and C. Keswani (eds), Advances in PGPR Research. Wallingford UK: CABI.
9.Orhan, F., & Gulluce, M. (2015). Isolation and characterization of salt-tolerant bacterial strains in salt-affected soils of Erzurum, Turkey. Geomicrobiology Journal, 32 (6), 521-529. doi: 10.1080/01490451.2014.962674.
10.Kumar, A., & Verma, J. P. (2018). Does plant—microbe interaction confer stress tolerance in plants: a review? Microbiological Research, 207, 41-52. doi:10.1016/j.micres.2017.11.004.
11.Abdelaal, K., AlKahtani, M., Attia, K., Hafez, Y., Király, L., & Künstler, A. (2021). The role of plant growth-promoting bacteria in alleviating the adverse effects of drought on plants. Biology, 10 (6), 520. doi:10.3390/ biology10060520.
12.Vurukonda, S. S. K. P., Vardharajula, S., Shrivastava, M., & SkZ, A. (2016). Enhancement of drought stress tolerance in crops by plant growth promoting rhizobacteria. Microbiological Research, 184, 13-24. doi:10.1016/j.micres.2015. 12.003.
13.Mapelli, F., Marasco, R., Rolli, E., Barbato, M., Cherif, H., Guesmi, A., Ouzari, I., Daffonchio, D., & Borin, S. (2013). Potential for plant growth promotion of rhizobacteria associated with Salicornia growing in Tunisian hypersaline soils. BioMed Research International, 2013, 1-13. doi:10.1155/ 2013/248078.
14.Chen, W., Lin, F., Lin, K. H., Chen, C., Xia, C., Liao, Q., Chen, S. P., & Kuo, Y. W. (2022). Growth promotion and salt-tolerance improvement of Gerbera jamesonii by root colonization of Piriformospora indica. Journal of Plant Growth Regulation, 41(3), 1219-1228. doi:10.1007/s00344-021-10385-4.
15.Shultana, R., Zuan, A. T. K., Naher, U. A., Islam, A. M., Rana, M. M., Rashid, M. H., Irin, I.J., Islam, S.S., Rim, A.A., & Hasan, A. K. (2022). The PGPR mechanisms of salt stress adaptation and plant growth promotion. Agronomy, 12 (10), 2266. doi:10.3390/ agronomy12102266.
16.Ilyas, N., Mazhar, R., Yasmin, H., Khan, W., Iqbal, S., Enshasy, H. E., & Dailin, D. J. (2020). Rhizobacteria isolated from saline soil induce systemic tolerance in wheat (Triticum aestivum L.) against salinity stress. Agronomy, 10 (7), 1-19. doi:10.3390/agronomy10070989.
17.Egamberdieva, D., Wirth, S. J., Alqarawi, A. A., Abd-Allah, E. F., & Hashem, A. (2017). Phytohormones and beneficial microbes: essential components for plants to balance stress and fitness. Frontiers in Microbiology, 8, 1-14. doi:10.3389/fmicb.2017.02104.
18.Gee, G. W., and Bauder, J. W. (1986). Particle‐size analysis. P 383-411, In: A. Klute (ed.), Methods of soil analysis: Physical and mineralogical methods. Soil Science Society of America Inc.
19.Jackson, M. (1967). Soil chemical analysis prentice. Hall of India Private Limited, New Delhi, 498p.
20.Naik, P. R., Raman, G., Narayanan, K. B., & Sakthivel, N. (2008). Assessment of genetic and functional diversity of phosphate solubilizing fluorescent pseudomonads isolated from rhizospheric soil. BMC Microbiology, 8 (1), 1-14. doi:10.1186/1471-2180-8-230.
21.M Atlas, R. 2010. Handbook of microbiological media. 1572p.
22.Chung, H., Park, M., Madhaiyan, M., Seshadri, S., Song, J., Cho, H., & Sa, T. (2005). Isolation and characterization of phosphate solubilizing bacteria from the rhizosphere of crop plants of Korea. Soil Biology and Biochemistry, 37 (10), 1970-1974. doi:10.1016/j. soilbio.2005.02.025.
23.Hu, X., Chen, J., & Guo, J. (2006). Two phosphate-and potassium-solubilizing bacteria isolated from Tianmu Mountain, Zhejiang, China. World Journal of Microbiology and Biotechnology, 22 (9), 983-990. doi:10.1007/s11274-006-9144-2.
24.Liang, Y., Xu, Z., Xu, Q., Zhao, X., Niu, S., & Yin, X. (2023). Isolation of Inorganic Phosphorus-solubilizing bacteria from the rhizosphere of Festuca arundinacea Schreb. Geomicrobiology Journal, 40 (6), 538-546. doi:10.1080/ 01490451.2023.2208096.
25.Goswami, D., Patel, K., Parmar, S., Vaghela, H., Muley, N., Dhandhukia, P., & Thakker, J. N. (2015). Elucidating multifaceted urease producing marine Pseudomonas aeruginosa BG as a cogent PGPR and bio-control agent. Plant Growth Regulation, 75, 253-263. doi: 10.1007/s10725-014-9949-1.
26.Mali, S. D., & Attar, Y. C. (2021). Formulation of cost-effective agro residues containing potassium solubilizing bacterial bio-inoculants using response surface methodology. Biocatalysis and Agricultural Biotechnology, 35, 102113. doi:10.1016/j.bcab.2021.102113.
27.Minas, K., McEwan, N. R., Newbold, C. J., & Scott, K. P. (2011). Optimization of a high-throughput CTAB-based protocol for the extraction of qPCR-grade DNA from rumen fluid, plant and bacterial pure cultures. FEMS Microbiology Letters, 325 (2), 162-169. doi:10.1111/j.1574-6968.2011.02424.x.
28.Sharma, S., Kulkarni, J., & Jha, B. (2016). Halotolerant rhizobacteria promote growth and enhance salinity tolerance in peanut. Frontiers in Microbiology, 7, 1600. doi:10.3389/fmicb.2016. 01600.
29.Tirry, N., Ferioun, M., Kouchou, A., Laghmari, G., Bahafid, W., & El Ghachtouli, N. (2022). Enhanced Salinity Tolerance of Medicago sativa, roots AM colonization and soil enzyme activities by PGPR. Environmental Sciences Proceedings, 16 (1), 14. doi: 10.3390/environsciproc2022016014.
30.Wang, W., Wu, Z., He, Y., Huang, Y., Li, X., & Ye, B. C. (2018). Plant growth promotion and alleviation of salinity stress in Capsicum annuum L. by Bacillus isolated from saline soil in Xinjiang. Ecotoxicology and Environmental Safety, 164, 520-529. doi:10.1016/j. ecoenv.2018.08.070
31.Salimi, A., Etemadi, M., Eshghi, S., Karami, A., & Alizargar, J. (2021). The effects of halomonas sp. and azotobacter sp. on ameliorating the adverse effect of salinity in purple basil (Ocimum basilicum l.). Preprints. 1, 1-27. doi:10.20944/preprints202106. 0391.v1.
32.Sagar, A., Rai, S., Ilyas, N., Sayyed, R. Z., Al-Turki, A. I., El Enshasy, H. A., & Simarmata, T. (2022). Halotolerant rhizobacteria for salinity-stress mitigation: Diversity, mechanisms and molecular approaches. Sustainability, 14 (1), 1-19. doi:10.3390/su14010490.
33.Zia, R., Nawaz, M. S., Yousaf, S., Amin, I., Hakim, S., Mirza, M. S., & Imran, A. (2021). Seed inoculation of desert‐plant growth‐promoting rhizobacteria induce biochemical alterations and develop resistance against water stress in wheat. Physiologia Plantarum, 172 (2), 990-1006. doi:10.1111/ppl.13362.
34.Yasmin, H., Nosheen, A., Naz, R., Keyani, R., & Anjum, S. 2019. Regulatory role of rhizobacteria to induce drought and salt stress tolerance in plants. P 279-335, In: Maheshwari, D., and Dheeman, S. (eds) Field Crops: Sustainable Management by PGPR. Sustainable Development and Biodiversity, Springer, Cham.
35.Sarkar, A., Ghosh, P. K., Pramanik, K., Mitra, S., Soren, T., Pandey, S., Mondal, M. H., & Maiti, T. K. (2018). A halotolerant Enterobacter sp. displaying ACC deaminase activity promotes rice seedling growth under salt stress. Research in Microbiology, 169 (1), 20-32. doi:10.1016/j.resmic.2017.08.005.
36.Singh, R. P., & Jha, P. N. (2016). The multifarious PGPR Serratia marcescens CDP-13 augments induced systemic resistance and enhanced salinity tolerance of wheat (Triticum aestivum L.). PLos One, 11 (6), 1-24. doi:10.1371/ journal.pone.0155026.
37.Kusale, S. P., Attar, Y. C., Sayyed, R. Z., Malek, R. A., Ilyas, N., Suriani, N. L., Khan, N., & El Enshasy, H. A. (2021). Production of plant beneficial and antioxidants metabolites by Klebsiella variicola under salinity stress. Molecules, 26 (7), 1-16. doi:10.3390/ molecules26071894.
38.Sunita, K., Mishra, I., Mishra, J., Prakash, J., & Arora, N. K. (2020). Secondary metabolites from halotolerant plant growth promoting rhizobacteria for ameliorating salinity stress in plants. Frontiers in Microbiology, 11, 1-12. doi:10.3389/fmicb.2020.567768.
39.Barbaccia, P., Gaglio, R., Dazzi, C., Miceli, C., Bella, P., Lo Papa, G., & Settanni, L. (2022). Plant Growth-Promoting Activities of Bacteria Isolated from an Anthropogenic Soil Located in Agrigento Province. Microorganisms, 10 (11), 1-13. doi: 10.3390/microorganisms10112167.
40.Amaresan, N., Kumar, K., Madhuri, K., & Usharani, G. K. (2016). Isolation and characterization of salt tolerant plant growth promoting rhizobacteria from plants grown in tsunami affected regions of Andaman and Nicobar Islands. Geomicrobiology Journal, 33 (10), 942-947. doi:10.1080/01490451.2015.1128994.
41.Remonsellez, F., Castro-Severyn, J., Pardo-Esté, C., Aguilar, P., Fortt, J., Salinas, C., Barahona, S., León, J., Fuentes, B., & Saavedra, C. P. (2018). Characterization and salt response in recurrent halotolerant Exiguobacterium sp. SH31 isolated from sediments of Salar de Huasco, Chilean Altiplano. Frontiers in Microbiology, 9, 1-17. doi:10.3389/fmicb.2018.02228.
42.Zhou, C., Zhu, L., Xie, Y., Li, F., Xiao, X., Ma, Z., & Wang, J. (2017). Bacillus licheniformis SA03 confers increased saline–alkaline tolerance in chrysanthemum plants by induction of abscisic acid accumulation. Frontiers in Plant Science, 8, 1-17. doi:10.3389/fpls.2017. 01143.
43.Upadhyay, S. K., & Singh, D. P. (2015). Effect of salt‐tolerant plant growth‐promoting rhizobacteria on wheat plants and soil health in a saline environment. Plant Biology, 17 (1), 288-293. doi:10.1111/plb.12173.
44.Albdaiwi, R. N., Khyami-Horani, H., Ayad, J. Y., Alananbeh, K. M., & Al-Sayaydeh, R. (2019). Isolation and characterization of halotolerant plant growth promoting rhizobacteria from durum wheat (Triticum turgidum subsp. durum) cultivated in saline areas of the dead sea region. Frontiers in Microbiology, 10, 1-16. doi:10.3389/ fmicb.2019.01639.
45.Liu, W., Hou, J., Wang, Q., Ding, L., & Luo, Y. (2014). Isolation and characterization of plant growth-promoting rhizobacteria and their effects on phytoremediation of petroleum-contaminated saline-alkali soil. Chemosphere, 117, 303-308. doi: 10.1016/ j.chemosphere.2014.07.026.
46.Liu, W., Wang, Q., Hou, J., Tu, C., Luo, Y., & Christie, P. (2016). Whole genome analysis of halotolerant and alkalotolerant plant growth-promoting rhizobacterium Klebsiella sp. D5A. Scientific Reports, 6 (1), 1-10. doi: 10.1038/srep26710.
47.Sapre, S., Gontia-Mishra, I., & Tiwari, S. (2018). Klebsiella sp. confers enhanced tolerance to salinity and plant growth promotion in oat seedlings (Avena sativa). Microbiological Research, 206, 25-32. doi:10.1016/ j.micres.2017.09.009.
48.Singh, R. P., Jha, P., & Jha, P. N. (2015). The plant-growth-promoting bacterium Klebsiella sp. SBP-8 confers induced systemic tolerance in wheat (Triticum aestivum) under salt stress. Journal of Plant Physiology, 184, 57-67. doi:10.1016/j.jplph.2015.07.002.
49.Drzewiecka, D. (2016). Significance and roles of Proteus spp. bacteria in natural environments. Microbial ecology,
72, 741-758. doi:10.1007/s00248-015-0720-6.
50.Jha, B., Gontia, I., & Hartmann, A. (2012). The roots of the halophyte Salicornia brachiata are a source of new halotolerant diazotrophic bacteria with plant growth-promoting potential. Plant and Soil, 356, 265-277. doi:10.1007/ s11104-011-0877-9.
51.Oliva, G., Di Stasio, L., Vigliotta, G., Guarino, F., Cicatelli, A., & Castiglione, S. (2023). Exploring the Potential of Four Novel Halotolerant Bacterial Strains as Plant-Growth-Promoting Rhizobacteria (PGPR) under Saline Conditions. Applied Sciences, 13 (7), 1-13. doi:10.3390/app13074320.
52.Mapelli, F., Marasco, R., Rolli, E., Barbato, M., Cherif, H., Guesmi, A., Ouzari, I., Daffonchio, D., & Borin, S. (2013). Potential for plant growth promotion of rhizobacteria associated with Salicornia growing in Tunisian hypersaline soils. BioMed Research International, 2013, 1-13. doi:10.1155/ 2013/248078.
53.Jiang, H., Wang, T., Chi, X., Wang, M., Chen, N., Chen, M., Pan, L., & Qi, P. (2020). Isolation and characterization of halotolerant phosphate solubilizing bacteria naturally colonizing the peanut rhizosphere in salt-affected soil. Geomicrobiology Journal, 37 (2), 110-118. doi:10.1080/01490451.2019.1666195.
54.Kashyap, B. K., Ara, R., Singh, A., Kastwar, M., Aaysha, S., Mathew, J., and Solanki, M. K. 2019. Halotolerant PGPR bacteria: Amelioration for salinity stress. P 509-530, In: D. Singh, V. Gupta, and R. Prabha (eds) Microbial Interventions in Agriculture and Environment. Springer, Singapore.
55.Safdarian, M., Askari, H., Nematzadeh, G., & Adriano, S. O. F. O. (2020). Halophile plant growth-promoting rhizobacteria induce salt tolerance traits in wheat seedlings (Triticum aestivum L.). Pedosphere, 30(5), 684-693. doi: 10.1016/S1002-0160(19)60835-0.
56.Mishra, P., Mishra, J., & Arora, N. K. (2021). Plant growth promoting bacteria for combating salinity stress in plants-Recent developments and prospects: A review. Microbiological Research, 252, 1-13. doi:10.1016/j.micres.2021. 126861.
57.Girma, B., Panda, A. N., Roy, P. C., Ray, L., Mohanty, S., & Chowdhary, G. (2022). Molecular, biochemical, and comparative genome analysis of a rhizobacterial strain Klebsiella Sp. KBG6. 2 imparting salt stress tolerance to Oryza sativa L. Environmental and Experimental Botany, 203, 1-13. doi: 10.1016/j.envexpbot.2022.105066.
58.Sultana, S., Alam, S., & Karim, M. M. (2021). Screening of siderophore-producing salt-tolerant rhizobacteria suitable for supporting plant growth in saline soils with iron limitation. Journal of Agriculture and Food Research, 4, 1-5. doi:10.1016/j.jafr.2021.100150.
59.Vandana, U. K., Singha, B., Gulzar, A. B. M., & Mazumder, P. B. 2020. Molecular mechanisms in plant growth promoting bacteria (PGPR) to resist environmental stress in plants. P 221-233, In: V. Sharma, R. Salwan, and L.K.T. Al. Ani, (eds), In Molecular aspects of plant beneficial microbes in agriculture, Elsevier, Academic Press.
60.Kour, D., Rana, K. L., Kaur, T., Yadav, N., Halder, S. K., Yadav, A. N., Sachan, S.G., & Saxena, A. K. 2020. Potassium solubilizing and mobilizing microbes: biodiversity, mechanisms of solubilization, and biotechnological implication for alleviations of abiotic stress. P 177-202, In:  A. A. Rastegari, A. N. Yadav, & N. Yadav (eds), In New and future developments in microbial biotechnology and bioengineering, Elsevier.
61.Raji, M., & Thangavelu, M. (2021). Isolation and screening of potassium solubilizing bacteria from saxicolous habitat and their impact on tomato growth in different soil types. Archives of Microbiology, 203(6), 3147-3161. doi:10.1007/s00203-021-02284-9.
62.Dong, X., Lv, L., Wang, W., Liu, Y., Yin, C., Xu, Q., Yan, H., Fu, J., & Liu, X. (2019). Differences in distribution of potassium-solubilizing bacteria in forest and plantation soils in Myanmar. International Journal of Environmental Research and Public Health, 16 (5), 1-14. doi:10.3390/ijerph16050700.
63.Susilowati, D. N., Sudiana, I., Mubarik, N. R., Agatis, J., & Campus, D. (2015). Species and functional diversity of rhizobacteria of rice plant in the coastal soils of Indonesia. Indonesian Journal of Agricultural Science. 16, 39-50. doi: 10.21082/IJAS.V16N1.2015.P39-50.
64.Duca, D., Lorv, J., Patten, C. L., Rose, D., & Glick, B. R. (2014). Indole-3-acetic acid in plant–microbe interactions. Antonie Van Leeuwenhoek, 106, 85-125. doi:10.1007/s10482-013-0095-y.
65.Saleem, S., Iqbal, A., Ahmed, F., & Ahmad, M. (2021). Phytobeneficial and salt stress mitigating efficacy of IAA producing salt tolerant strains in Gossypium hirsutum. Saudi Journal of Biological Sciences, 28 (9), 5317-5324. doi:10.1016/j.sjbs.2021.05.056.
Journal of Soil Management and Sustainable Production
Volume 13, Issue 3
September 2023
Pages 100-115

Files

Share

How to cite

Statistics