Abstract
Bacteria that solubilize nutrients in the soil are commonly used as bio-inoculants for promoting the growth of different crop species. However, the influence of potassium (K) solubilizing bacteria (KSB) originating from saxicolous habitat (rock-dwelling) on plant growth has not been frequently examined. In this study, we isolated KSB from saxicolous habitats and estimated their ability to produce plant growth hormone, organic acids, and siderophore that may facilitate plant growth. Fifteen culturable saxicolous bacterial isolates with varied K solubilizing ability were isolated from two sites. Of these, four potential K solubilizers were selected and identified by 16S rRNA gene sequencing. The four bacterial isolates resembled Bacillus subtilis, Bacillus cereus, Bacillus licheniformis, and Burkholderia cenocepacia and produced different organic acids, indole acetic acid, and siderophore under in vitro conditions. Potassium solubilization differed among the bacterial isolates and was significantly influenced by K sources. Inoculation of KSB improved the tomato plant growth parameters like plant height, leaf area, total root length, root/shoot ratio, and tissue K content in sterilized and unsterilized Alfisol, and Vertisol soils under greenhouse conditions. We also observed higher residual K content in the KSB inoculated post-harvest soils. Among the four KSB isolates screened, B. licheniformis and B. cenocepacia presents an excellent prospect as bio-inoculants for improving tomato growth in different soil types. Besides these, the enriched K content in the post-harvest soils may help the growth of subsequent crops in sustainable agriculture.
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References
Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 26:1–20. https://doi.org/10.1016/j.jksus.2013.05.001
Altieri MA, Nicholls CI, Montalba R (2017) Technological approaches to sustainable agriculture at a crossroads: an agroecological perspective. Sustainability 9:349. https://doi.org/10.3390/su9030349
Anjanadevi IP, John NS, John KS, Jeeva ML, Misra RS (2016) Rock inhabiting potassium solubilizing bacteria from Kerala, India: characterization and possibility in chemical K fertilizer substitution. J Basic Microbiol 56:67–77. https://doi.org/10.1002/jobm.201500139
Arora NK, Verma M (2017) Modified microplate method for rapid and efficient estimation of siderophore produced by bacteria. 3 Biotech 7:381. https://doi.org/10.1007/s13205-017-1008-y
Bagyalakshmi B, Ponmurugan P, Balamurugan A (2017) Potassium solubilization, plant growth promoting substances by potassium solubilizing bacteria (KSB) from southern Indian tea plantation soil. Biocatal Agric Biotechnol 12:116–124. https://doi.org/10.1016/j.bcab.2017.09.011
Bakhshandeh E, Rahimian H, Pirdashti H, Nematzadeh G (2015) Evaluation of phosphate solubilizing bacteria on the growth and grain yield of rice (Oryza sativa L.) cropped in northern Iran. J Appl Microbiol 119:1371–1382. https://doi.org/10.1111/jam.12938
Bakhshandeh E, Pirdashti H, Lendeh KS (2017) Phosphate and potassium-solubilizing bacteria effect on the growth of rice. Ecol Eng 103:164–169. https://doi.org/10.1016/j.ecoleng.2017.03.008
Ben Zineb A, Trabelsi D, Ayachi I, Barhoumi F, Aroca R, Mhamdi R (2020) Inoculation with elite strains of phosphate solubilizing bacteria enhances the effectiveness of fertilization with rock phosphates. Geomicrobiol J 37:22–30. https://doi.org/10.1080/01490451.2019.1658826
Bharti N, Yadav D, Barnawal D, Maji D, Kalra A (2013) Exiguobacterium oxidotolerans, a halotolerant plant growth promoting rhizobacteria, improves yield and content of secondary metabolites in Bacopa monnieri (L.) Pennell under primary and secondary salt stress. World J Microbiol Biotechnol 29:379–387. https://doi.org/10.1007/s11274-012-1192-1
Bhattacharya S, Bachani P, Jain D, Patidar SK, Mishra S (2016) Extraction of potassium from K-feldspar through potassium solubilization in the halophilic Acinetobacter soli (MTCC 5918) isolated from the experimental salt farm. Int J Miner Process 152:53–57. https://doi.org/10.1016/j.minpro.2016.05.00
Brewer TE, Fierer N (2017) Tales from the tomb: the microbial ecology of exposed rock surfaces. Environ Microbiol 20:958–970. https://doi.org/10.1111/1462-2920.14024
Brupbacher RH (1968) Analytical methods and procedures used in the soil testing laboratory. LSU Agricultural Experiment Station Reports 454:1–28
Buragohain S, Nath DJ, Devi YB, Bhattacharyya B, Dutta S (2018) Molecular characterization of potassium solubilizing bacteria from crop rhizosphere of the North Eastern Region of India. Curr Sci 114:2543. https://doi.org/10.18520/cs/v114/i12/2543-2548
Di Benedetto NA, Corbo MR, Campaniello D, Cataldi MP, Bevilacqua A, Sinigaglia M, Flagella Z (2017) The role of plant growth promoting bacteria in improving nitrogen use efficiency for sustainable crop production: a focus on wheat. AIMS Microbiol 3:413. https://doi.org/10.3934/microbiol.2017.3.413
Egamberdiyeva D (2007) The effect of plant growth promoting bacteria on growth and nutrient uptake of maize in two different soils. Appl Soil Ecol 36:184–189. https://doi.org/10.1016/j.apsoil.2007.02.005
Engindeniz S, Cosar GO (2013) An economic comparison of pesticide applications for processing and table tomatoes: a case study for Turkey. J Plant Prot Res 53:230–237. https://doi.org/10.2478/jppr-2013-0035
Eshghi S, Safizadeh MR, Jamali B, Sarseifi M (2012) Influence of foliar application of volk oil, dormex, gibberellic acid and potassium nitrate on vegetative growth and reproductive characteristics of strawberry cv. ‘Merak.’ J Biol Environ Sci 6:35–38
Fanourakis D, Briese C, Max JFJ, Kleinen S, Putz A, Fiorani F, Ulbrich A, Schurr U (2014) Rapid determination of leaf area and plant height by using light curtain arrays in four species with contrasting shoot architecture. Plant Methods 10:9. https://doi.org/10.1186/1746-4811-10-9
FAOSTAT (2018) Food and Agriculture organization of the United Nations. http://faostat.fao.org. Accessed 2018 Aug
Ferreira MJ, Silva H, Cunha A (2019) Siderophore-producing rhizobacteria as a promising tool for empowering plants to cope with iron limitation in saline soils: a review. Pedosphere 29:409–420. https://doi.org/10.1016/s1002-0160(19)60810-6
Girgis MGZ, Khalil HMA, Sharaf MS (2008) In vitro evaluation of rock phosphate and potassium solubilizing potential of some Bacillus strains. Aus J Basic Appl Sci 2:68–81
Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica. https://doi.org/10.6064/2012/963401
Han H, Lee K (2005) Phosphate and potassium solubilizing bacteria effect on mineral uptake, soil availability and growth of eggplant. Res J Agric Biol Sci 1:176–180
Han H, Lee K (2006) Effect of co-inoculation with phosphate and potassium solubilizing bacteria on mineral uptake and growth of pepper and cucumber. Plant Soil Environ 52:130–136
Heffer P, Prud’homme M (2014) Fertilizer Outlook 2014–2018. Paris, France: International Fertilizer Industry Association (IFA)
Hu X, Chen J, Guo J (2006) Two phosphate-and potassium-solubilizing bacteria isolated from Tianmu Mountain, Zhejiang, China. World J Microbiol Biotechnol 22:983–990. https://doi.org/10.1007/s11274-006-9144-2
Irizarry I, White JF (2017) Application of bacteria from non-cultivated plants to promote growth, alter root architecture and alleviate salt stress of cotton. J Appl Microbiol 122:1110–1120. https://doi.org/10.1111/jam.13414
Jackson M (1973) Soil chemical analysis. Pentice Hall of India Pvt. Ltd, New Delhi
Keshavarz Zarjani J, Aliasgharzad N, Oustan S, Emadi M, Ahmadi A (2013) Isolation and characterization of potassium solubilizing bacteria in some Iranian soils. Arch Agron Soil Sci 59:1713–1723. https://doi.org/10.1080/03650340.2012.756977
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120. https://doi.org/10.1007/BF01731581
Koseki S, Nonaka J (2012) Alternative approach to modeling bacterial lag time, using logistic regression as a function of time, temperature, pH, and sodium chloride concentration. Appl Environ Microbiol 78:6103–6112. https://doi.org/10.1128/AEM.01245-12
Kraemer SM (2004) Iron oxide dissolution and solubility in the presence of siderophores. Aquat Sci 66:3–18. https://doi.org/10.1007/s00027-003-0690-5
Kumar A, Maurya B, Raghuwanshi R (2014) Isolation and characterization of PGPR and their effect on growth, yield and nutrient content in wheat (Triticum aestivum L.). Biocatal Agric Biotechnol 3:121–128. https://doi.org/10.1016/j.bcab.2014.08.003
Liu W, Xu X, Wu X, Yang Q, Luo Y, Christie P (2006) Decomposition of silicate minerals by Bacillus mucilaginosus in liquid culture. Environ Geochem Health 28:133–140. https://doi.org/10.1007/s10653-005-9022-0
Liu Z, Wang H, Xu W, Wang Z (2020) Isolation and evaluation of the plant growth promoting rhizobacterium Bacillus methylotrophicus (DD-1) for growth enhancement of rice seedling. Arch Microbiol. https://doi.org/10.1007/s00203-020-01934-8
Lower SK (2001) Bacterial recognition of mineral surfaces: Nanoscale interactions between shewanella and alpha -FeOOH. Science 292:1360–1363. https://doi.org/10.1126/science.1059567
Manjunath M, Kanchan A, Ranjan K, Venkatachalam S, Prasanna R, Ramakrishnan B, Singh B (2016) Benefcial cyanobacteria and eubacteria synergistically enhance bioavailability of soil nutrients and yield of okra. Heliyon 2:10–16. https://doi.org/10.1016/j.heliyon.2016.e00066
Meena VS, Maurya B, Verma JP (2014) Does a rhizospheric microorganism enhance K+ availability in agricultural soils? Microbiol Res 169:337–347. https://doi.org/10.1016/j.micres.2013.09.003
Meena VS, Maurya BR, Verma JP, Aeron A, Kumar A, Kim K, Bajpai VK (2015) Potassium solubilizing rhizobacteria (KSR): Isolation, identification, and K-release dynamics from waste mica. Ecol Eng 81:340–347. https://doi.org/10.1016/j.ecoleng.2015.04.065
Olanrewaju OS, Glick BR, Babalola OO (2017) Mechanisms of action of plant growth promoting bacteria. World J Microbiol Biotechnol. https://doi.org/10.1007/s11274-017-2364-9
Onyia CO, Okoh AM, Irene O (2020) Production of plant growth promoting bacteria biofertilizer from organic waste material and evaluation of its performance on the growth of corn (Zea mays). Am J Plant Sci 11:189–200. https://doi.org/10.4236/ajps.2020.112015
Park M, Singvilay O, Seok Y, Chung J, Ahn K, Sa T (2003) Effect of phosphate solubilizing fungi on P uptake and growth to tobacco in rock phosphate applied soil. Korean J Soil Sci Fertil 36:233–238
Parmar P, Sindhu SS (2018) The novel and efficient method for isolating potassium solubilizing bacteria from rhizosphere soil. Geomicrobiol J 36:130–136. https://doi.org/10.1080/01490451.2018.1514442
Pérez-Flores P, Valencia-Cantero E, Altamirano-Hernández J, Pelagio-Flores R, López-Bucio J, García-Juárez P, Macías-Rodríguez L (2017) Bacillus methylotrophicus M4–96 isolated from maize (Zea mays) rhizoplane increases growth and auxin content in Arabidopsis thaliana via emission of volatiles. Protoplasma 254:2201–2213. https://doi.org/10.1007/s00709-017-1109-9
Pramanik P, Goswami A, Ghosh S, Kalita C (2019) An indigenous strain of potassium-solubilizing bacteria Bacillus pseudomycoides enhanced potassium uptake in tea plants by increasing potassium availability in the mica waste-treated soil of Northeast India. J Appl Microbiol 126:215–222. https://doi.org/10.1111/jam.14130
Premono ME, Moawad AM, Vleck PLG (1996) Effect of phosphate solubilizing Pseudomonas putida on the growth of maize and its survival in the rhizosphere. Indones J Agric Sci 11:13–23
Qureshi SA, Qureshi RA, Sodha AB, Tipre DR, Dave SR (2018) Bioextraction dynamics of potassium from feldspar by heterotrophic microorganisms isolated from ceramic and rhizospheric soil. Geomicrobiol J 35:127–131. https://doi.org/10.1080/01490451.2017.1338797
Ramamurthy V, Naidu L, Chary GR, Mamatha D, Singh S (2017) Potassium status of Indian soils: need for rethinking in research, recommendation and policy. Int J Curr Microbiol App Sci 6:1529–1540. https://doi.org/10.20546/ijcmas.2017.612.171
Saha M, Maurya BR, Meena VS, Bahadur I, Kumar A (2016) Identification and characterization of potassium solubilizing bacteria (KSB) from Indo-Gangetic Plains of India. Biocatal Agric Biotechnol 7:202–209. https://doi.org/10.1016/j.bcab.2016.06.007
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Sarikhani MR, Oustan S, Ebrahimi M, Aliasgharzad N (2018) Isolation and identification of potassium-releasing bacteria in soil and assessment of their ability to release potassium for plants. Eur J Soil Sci. https://doi.org/10.1111/ejss.12708
Schwartz AR, Ortiz I, Maymon M, Herbold CW, Fujishige NA, Vijanderan JA, Villella W, Hanamoto K, Diener A, Sanders ER, DeMason DA, Hirsch AM (2013) Bacillus simplex—a little known PGPB with anti-fungal activity—alters pea legume root architecture and nodule morphology when coinoculated with Rhizobium leguminosarum bv. viciae. Agronomy 3:595–620. https://doi.org/10.3390/agronomy3040595
Shirale AO, Meena BP, Gurav PP, Srivastava S, Biswas AK, Thakur JK, Somasundaram J, Patra AK, Rao AS (2019) Prospects and challenges in utilization of indigenous rocks and minerals as source of potassium in farming. J Plant Nutr 42:2682–2701. https://doi.org/10.1080/01904167.2019.1659353
Sultana R, Dilruba S, Parvin N, Islam ABMJ (2015) Effect of Potassium on growth and yield of Tomato (Lycopersicon esculentum Mill.). Eco-friendly Agric J 8:77–80
Takehisa H, Sato Y, Antonio BA, Nagamura Y (2013) Global transcriptome profile of rice root in response to essential macronutrient deficiency. Plant Signal Behav 8:e24409. https://doi.org/10.4161/psb.24409
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. https://doi.org/10.1093/molbev/msr121
Tennant D (1975) A test of a modified line intersect method of estimating root length. J Ecol. https://doi.org/10.2307/2258617
Uroz S, Kelly LC, Turpault M-P, Lepleux C, Frey-Klett P (2015) The Mineralosphere concept: mineralogical control of the distribution and function of mineral-associated bacterial communities. Trends Microbiol 23:751–762. https://doi.org/10.1016/j.tim.2015.10.004
Vazquez P, Holguin G, Puente M, Lopez-Cortes A, Bashan Y (2000) Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves in a semiarid coastal lagoon. Biol Fertil Soils 30:460–468. https://doi.org/10.1007/s003740050024
Vicente-Hernández A, Salgado-Garciglia R, Valencia-Cantero E, Ramírez-Ordorica A, Hernández-García A, García-Juárez P, Macías-Rodríguez L (2019) Bacillus methylotrophicus M4–96 Stimulates the Growth of Strawberry (Fragaria × ananassa “Aromas”) plants in vitro and slows Botrytis cinerea infection by two different methods of interaction. J Plant Growth Regul 38:765–777. https://doi.org/10.1007/s00344-018-9888-6
Vyas P, Gulati A (2009) Organic acid production in vitro and plant growth promotion in maize under controlled environment by phosphate-solubilizing fluorescent Pseudomonas. BMC Microbiol 9:174. https://doi.org/10.1186/1471-2180-9-174
Wu Y, Zhang J, Wang L, Wang Y (2017) A rock-weathering bacterium isolated from rock surface and its role in ecological restoration on exposed carbonate rocks. Ecol Eng 101:162–169. https://doi.org/10.1016/j.ecoleng.2017.01.023
Xiao Y, Wang X, Chen W, Huang Q (2017) Isolation and identification of three potassium-solubilizing bacteria from rape rhizospheric soil and their effects on ryegrass. Geomicrobiol J 34:873–880. https://doi.org/10.1080/01490451.2017.1286416
Zhang C, Kong F (2014) Isolation and identification of potassium-solubilizing bacteria from tobacco rhizospheric soil and their effect on tobacco plants. Appl Soil Ecol 82:18–25. https://doi.org/10.1016/j.apsoil.2014.05.002
Zhao Y, Zhang M, Yang W, Di HJ, Ma L, Liu W, Li B (2019) Effects of microbial inoculants on phosphorus and potassium availability, bacterial community composition, and chili pepper growth in a calcareous soil: a greenhouse study. J Soils Sediments 19:3597–3607. https://doi.org/10.1007/s11368-019-02319-1
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RM gratefully acknowledges the financial support in the form of Rajiv Gandhi National Fellowship from UGC, New Delhi (Grant no. F1−17.1/2016-17/RGNF-2015-17-SC-TAM−19396).
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This research was performed and written by RM. Designing the experiments and final editing of the manuscript was done by TM and RM.
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Raji, M., Thangavelu, M. Isolation and screening of potassium solubilizing bacteria from saxicolous habitat and their impact on tomato growth in different soil types. Arch Microbiol 203, 3147–3161 (2021). https://doi.org/10.1007/s00203-021-02284-9
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DOI: https://doi.org/10.1007/s00203-021-02284-9