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Characterization of zinc solubilization potential of arsenic tolerant Burkholderia spp. isolated from rice rhizospheric soil

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Abstract

In this study, experiments were conducted to isolate, characterize, and evaluate rice rhizosphere bacteria for their arsenic (As) tolerance ability and zinc (Zn) solubilization potential in culture media and soil. Among 20 bacterial isolates recovered, six were found to solubilize inorganic Zn salt(s) efficiently under in vitro culture conditions. 16S rRNA gene sequence-based phylogenetic analysis indicated the affiliation of efficient Zn solubilizing bacteria (ZSB) to Burkholderia vietnamiensis and Burkholderia seminalis. Zinc solubilizing efficiency (ZSE) of the bacteria varied with the concentrations and types of Zn salts used in the experiments. Increasing trend in ZSE of the bacteria was noticed when the percentage of ZnO increased from 0.1 to 0.5 but the same decreased at 1.0%. Increased Zn solubilization was noticed when bacteria were incubated with lower concentration of Zn3(PO4)2 and ZnCO3. In general, Zn solubilization increased with increasing incubation time in lower volume medium, while some isolates failed to solubilize one or more tested Zn salts. However, enriched concentrated cells of the ZSB in glucose amended medium with 0.5% ZnO showed an increasing trend of Zn solubilization with time and were able to solubilize more than 300 mg/L Zn. This increased rate of Zn release by the ZSB was attributed to marked decline in pH that might be due to the enhanced gluconic acid production from glucose. As evident from the decreased ZSE of the bacteria in the presence of As(V) in particular, it seems arsenic imparts a negative effect on Zn solubilization. The ZSB were also able to increase the rate of Zn release in soil. A microcosm-based soil incubation study amending the enriched bacteria and 0.5% ZnO in soil showed an elevated level of both water-soluble and available Zn compared to un-inoculated control. During Zn solubilization in microcosms, viable cells in terms of colony-forming unit (CFU) declined by the same order of magnitude both in the presence and absence of ZnO that might be due to the nutrients limiting condition aroused during the incubation period rather than Zn toxicity. The bacteria in this study also exhibited plant growth promoting traits, such as growth in nitrogen-free medium, production of indole acetic acid (IAA), and solubilization of potassium and phosphate. Our findings suggested that Burkholderia spp. could be the potential candidates for enhancing Zn dissolution in the soil that might reduce the rate of inorganic Zn fertilization in agricultural soil.

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References

  • Abou-Shanab RA, vanBerkum P, Angle JS (2007) Heavy metal resistance and genotypic analysis of metal resistance genes in grampositive and gram-negative bacteria present in Ni-rich serpentine soil and in the rhizosphere of Alyssum murale. Chemosphere 68:360–367

    Article  CAS  Google Scholar 

  • Ahmed AMA, Ahmed G, Magda MH, TawfikIntegrated MM (2011) Effect of organic and biofertilizers on wheat productivity in new reclaimed soils. Res J Agric Biol Sci 7:105–114

    Google Scholar 

  • Andreini C, Bertini I, Rosato A (2009) Metalloproteomes: a bioinformatic approach. AccChem Res 42:1471–1479

    Article  CAS  Google Scholar 

  • Araújo FD, Araújo WL, Eberlin MN (2017) Potential of Burkholderia seminalis TC342R3 as biocontrol agent against Fusariumoxysporum evaluated by mass spectrometry imaging. J Am Soc Mass Spectrom 28:901. https://doi.org/10.1007/s13361-017-1610-6

    Article  CAS  PubMed  Google Scholar 

  • Alloway BJ (2009) Soil factors associated with zinc deficiency in crops and humans. Environ Geochem Health 31:537–548

    Article  CAS  Google Scholar 

  • Bapiri A, Asgharzadeh A, Mujallali H, Khavazi K, Pazira E (2012) Evaluation of zinc solubilization potential by different strains of fluorescent pseudomonads. J Appl Sci Environ Manag 16:295–298

    CAS  Google Scholar 

  • Bashri G, Patel A, Singh R, Parihar P, Prasad SM (2017) Mineral solubilization by microorganism: mitigating strategy in mineral deficient soil. Microbial Biotechnol. https://doi.org/10.1007/978-981-10-6847-8_12

    Article  Google Scholar 

  • Bhakat K, Chakraborty A, Islam E (2019) Characterization of arsenic oxidation and uranium bioremediation potential of arsenic resistant bacteria isolated from uranium ore. Environ Sci Pollut R 26:12907–12919. https://doi.org/10.1007/s11356-019-04827-6

    Article  CAS  Google Scholar 

  • Brocklehurst KR, Morby AP (2000) Metal-ion tolerance in Escherichia coli: analysis of transcriptional profiles by gene-array technology. Microbiology 146:2277–2282. https://doi.org/10.1099/00221287-146-9-2277

    Article  CAS  PubMed  Google Scholar 

  • Chakraborty A, Bhakat K, Islam E (2017) Arsenic contamination in agricultural soil reduces metabolic activity of total and free-living nitrogen-fixing bacteria as revealed by real-time qPCR. Soil Sediment Contam 26:736–748

    Article  CAS  Google Scholar 

  • Chakraborty A, Islam E (2018) Temporal dynamics of total and free-living nitrogen-fixing bacterial community abundance and structure in soil with and without history of arsenic contamination during a rice growing season. Environ Sci Pollut Res 25:4951–4962. https://doi.org/10.1007/s11356-017-0858-5

    Article  CAS  Google Scholar 

  • Coenye T, Goris J, Spilker T et al (2002) Characterization of unusual bacteria isolated from respiratory secretions of cystic fibrosis patients and description of Inquilinuslimosus gen nov., sp. nov. J Clin Microbiol 40(6):2062–2069

    Google Scholar 

  • Costerousse B, Schönholzer-Mauclaire L, Frossard E, Thonar C (2018) Identification of heterotrophic zinc mobilization processes among bacterial strains isolated from wheat rhizosphere (TriticumaestivumL.). Appl Environ Microbiol 84:01715–01717. https://doi.org/10.1128/AEM.01715-17

    Article  Google Scholar 

  • Deris ZZ, Van Rostenberghe H, Habsah H et al (2010) First isolation of Burkholderiatropica from a neonatal patient successfully treated with imipenem. Int J Infect Dis 14(1):e73–e74

    Article  Google Scholar 

  • Dinesh R, Srinivasan V, Hamza S, Sarathambal C, Gowda SA, Ganeshamurthy AN, Gupta SB, Nair VA, Subila KP, Lijina A, Divya VC (2018) Isolation and characterization of potential Zn solubilizing bacteria from soil and its effects on soil Zn release rates, soil available Zn and plant Zn content. Geoderma 321:173–186

    Article  CAS  Google Scholar 

  • Eberl L, Vandamme P (2016) Members of the genus Burkholderia: good and bad guys. F1000Research, 5, F1000 Faculty Rev-1007. https://doi.org/https://doi.org/10.12688/f1000research.8221.1

  • Estrada-delos Station P, Bustitio-Cristales R, Caballero-Mallado J (2001) Burkholderia, a genus rich in plant-associated nitrogen fixers with wide environmental and geographic distribution. Appl Environ Microbiol 67:279–2798

    Google Scholar 

  • Fasim F, Ahmed N, Parsons R, Gadd GM (2002) Solubilization of zinc salts by a bacterium isolated from the air environment of a tannery. FEMS Microbiol Lett 213:1–6

    Article  CAS  Google Scholar 

  • Figueiredo MV, Burity HA, Martı´nez CR, Chanway CP (2008) Alleviation of drought stress in the common bean (Phaseolus vulgaris L) by co-inoculation with Paenibacillus polymyxa and Rhizobium tropici. Appl Soil Ecol 40:182188

    Article  Google Scholar 

  • Gandhi A, Muralidharan G (2016) Assessment of zinc solubilizing potentiality of Acinetobacter sp. isolated from rice rhizosphere. Eur J Soil Biol 76:1–8

    Article  CAS  Google Scholar 

  • Gerrits GP, Klaassen C, Coenye T et al (2005) Burkholderia fungorum septicemia. Emerg Infect Dis 11(7):1115–1117

    Article  Google Scholar 

  • Gillis M, Van TV, Bardin R, Goor M, Hebbar P, Willems A, Segers P, Kersters K, Heulin T, Fernandez MP (1995) Polyphasic taxonomy in the genus Burkholderia leading to an emended description of the genus and proposition of Burkholderia vietnamiensis sp. nov for N2-fixing isolates from rice in Vietnam. Int J Syst Bacteriol 45:274–289

    Article  CAS  Google Scholar 

  • Gontia-Mishra I, Sapre S, Tiwari S (2017) Zinc solubilizing bacteria from the rhizosphere of rice as prospective modulator of zinc biofortification in rice. Rhizosphere 3:185–190

    Article  Google Scholar 

  • Goswami D, Parmar S, Vaghela H, Dhandhukia P, Thakker J (2015) Describing Paenibacillus mucilaginosus strain N3 as an efficient plant growth promoting rhizobacteria (PGPR). Cogent Food Agric 1:1000714

    Article  Google Scholar 

  • Govindarajan M, Balandreau J, Kwon S-W, Weon H-Y, Lakshminarasimhan C (2008) Effects of the inoculation of Burkholderia vietnamensis and related endophyticdiazotrophic bacteria on grain yield of rice. MicrobEcol 55:21–37

    Google Scholar 

  • Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plantbacterium signaling processes. Soil Biol Biochem 37:395412

    Article  Google Scholar 

  • Hendershot WH, Lalande H, Duquette M (2007) Soil Reaction and Exchangeable Acidity. In M. R. Carter and E. G. Gregorich, editors. Soil sampling and methods of analysis. Second edition. CRC Press, Taylor & Francis Group, Boca Raton, Florida, USA.

  • Hotz C, Brown KH (2004) Assessment of the risk of zinc deficiency in populations and options for its control. Food Nutr Bull 25:94–204

    Google Scholar 

  • Hu XF, Chen J, Guo JF (2006) Two phosphate-and potassium-solubilizing bacteria isolated from Tianmu Mountain, Zhejiang, China. World J Microbiol Biotechnol 22:983–990

    Article  CAS  Google Scholar 

  • Kamran S, Shahid I, Baig DN, Rizwan M, Malik KA, Mehnaz S (2017) Contribution of zinc solubilizing bacteria in growth promotion and zinc content of wheat. Front Microbiol 8:2593. https://doi.org/10.3389/fmicb.2017.02593

    Article  PubMed  PubMed Central  Google Scholar 

  • Kanwar JS (1973) Soil Fertility-Theory and Practice. Publ. Indian Council of Agricultural Research, New Delhi.

  • Katyal JC, Sharma BD (1991) DTPA extractable and total Zn, Cu, Mn and Fe in Indian soils. Geoderma 49:165–179

    Article  CAS  Google Scholar 

  • Khanghahi MY, Ricciuti P, Allegretta I, Terzano R, Crecchio C (2018) Solubilization of insoluble zinc compounds by zinc solubilizing bacteria (ZSB) and optimization of their growth conditions. Environ Sci Pollut Res 25:25862–25868

    Article  CAS  Google Scholar 

  • Krithika S, Balachandar D (2016) Expression of zinc transporter genes in rice as influenced by zinc-solubilizing Enterobacter cloacae strain ZSB14. Front Plant Sci 7:446

    Article  Google Scholar 

  • Kumar A, Dewangan S, Lawate P, Bahadur I, Prajapati S (2019) Zinc-Solubilizing Bacteria: A Boon for Sustainable Agriculture. Microorganisms for Sustainability. Plant Growth Promoting Rhizobacteria for Sustainable Stress Management https://doi/org/https://doi.org/10.1007/978-981-13-6536-2_8

  • Lee LJ, Barrett JA, Poole RK (2005) Genome-wide transcriptional response of chemostat cultured Escherichia coli to zinc. J Bacteriol 187:1124–1134. https://doi.org/10.1128/JB.187.3.1124-1134.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Ren X, Fan B, Huang Z, Wang W, Zhou H, Lou Z, Ding H, Lyu J, Tan G (2019) Zinc toxicity and iron-sulfur cluster biogenesis in Escherichia coli. Appl Environ Microbiol 85:01967–02018. https://doi.org/10.1128/AEM.01967-18

    Article  Google Scholar 

  • Li WC, Ye ZH, Wong MH (2010) Metal mobilization and production of short-chain organic acids by rhizosphere bacteria associated with a Cd/Zn hyperaccumulating plant, Sedum alfredii. Plant Soil 326:453–467

    Article  CAS  Google Scholar 

  • Louden BC, Haarmann D, Lynne AM (2011) Use of blue agar CAS assay for siderophore detection. J Microbiol Biol Educ 12:51–53

    Google Scholar 

  • Mumtaz MZ, Ahmad M, Jamil M, Hussain T (2017) Zinc solubilizing Bacillus spp. potential candidates for biofortification in maize. Microbiol Res 202:51–60

    Article  CAS  Google Scholar 

  • Nahas E (1996) Factors determining rock phosphate solubilization by microorganisms isolated from soil. World J Microbiol Biotechnol 12(6):567–572

    Article  CAS  Google Scholar 

  • Othman NMI, Othman R, Saud HM, Wahab PEM (2017) Effects of root colonization by zinc-solubilizing bacteria on rice plant (Oryza sativa MR219) growth. Agric Nat Resour 51:532–537

    Google Scholar 

  • Pikovskaya RI (1948) Mobilization of phosphorus in soil connection with the vital activity of some microbial species. Microbiology 17:362–370

    CAS  Google Scholar 

  • Ponnamperuma FN, Caylon MT, Lantin RS (1981) Dilute hydrochloric acid as an extractant for available zinc, copper and boron in rice soils. Plant Soil 61:291–310

    Article  Google Scholar 

  • Ramesh A, Sharma SK, Sharma MP, Yadav N, Joshi OP (2014) Inoculation of zinc solubilizing Bacillus aryabhattai strains for improved growth, mobilization and biofortification of zinc in soybean and wheat cultivated in vertisols of central India. Appl Soil Ecol 73:87–96

    Article  Google Scholar 

  • Rattan RK, Shukla LM (1984) Critical limits of deficiency and toxicity of zinc in paddy in a typic Ustipsamment. Commun Soil Sci Plant Anal 15(9):1041–1050. https://doi.org/10.1080/00103628409367541

    Article  CAS  Google Scholar 

  • Rokhbakhsh-Zamin F, Sachdev D, Kazemi-Pour N, Engineer A, Pardesi KR, Zinjarde S, Dhakephalkar PK, Chopade BA (2011) Characterization of plant-growth-promoting traits of Acinetobacter species isolated from rhizosphere of Pennisetumglaucum. J Microbiol Biotechnol 21:556–566

    Google Scholar 

  • Saravanan VS, Madhaiyan M, Thangaraju M (2007) Solubilization of zinc compounds by the diazotrophic, plant growth promoting bacterium Gluconacetobacter diazotrophicus. Chemosphere 66:1794–1798

    Article  CAS  Google Scholar 

  • Sawar M, Kremer RJ (1995) Determination of bacterially derived auxins using a microplate method. Lett Appl Microbiol 20:282–285

    Google Scholar 

  • Shaikh S, Saraf M (2017) Biofortification of Triticum aestivum through the inoculation of zinc solubilizing plant growth promoting rhizobacteria in field experiment. Biocatal Agric Biotechnol 9:120–126

    Google Scholar 

  • Shakeel M, Rais A, Hassan MN, Hafeez FY (2015) Root associated Bacillus sp improves growth, yield and zinc translocation for Basmati Rice (Oryza sativa) varieties. Front Microbiol 6:1286. https://doi.org/10.3389/fmicb.2015.01286

    Article  PubMed  PubMed Central  Google Scholar 

  • Sharma SK, Sharma MP, Ramesh A, Joshi OP (2012) Characterization of zinc-solubilizing Bacillus isolates and their potential to influence zinc assimilation in soybean seeds. J Microbiol Biotechnol 22:352–359. https://doi.org/10.4014/jmb.1106.05063

    Article  CAS  Google Scholar 

  • Sharma A, Patni B, Shankhdhar D, Shankhdhar SC (2013) Zinc - an indispensable micronutrient. Physiol Mol Biol Plants 19:11–20. https://doi.org/10.1007/s12298-012-0139-1

    Article  CAS  Google Scholar 

  • Shinjo R, Uesaka K, Ihara K, Sakazaki S, Yano K, Kondo M, Tanaka A (2018) Draft genome sequence of Burkholderia vietnamiensis strain RS1, a nitrogen-fixing endophyte isolated from sweet potato. Microbiol Resour Announc 7:00820–00918. https://doi.org/10.1128/MRA.00820-18

    Article  Google Scholar 

  • Vidyashree DN, Muthuraju R, Panneerselvam P, Saritha B, Ganeshamurthy AN (2016) Isolation and characterization of zinc solubilizing bacteria from stone quarry dust powder. Int J Agri Sci 8:3078–3081

    Google Scholar 

  • Wu TY, Gruissem W, Bhullar NK (2019) Targeting intracellular transport combined with efficient uptake and storage significantly increases grain iron and zinc levels in rice. Plant Biotechnol J 17:9–20

    Article  CAS  Google Scholar 

  • Zhang X, Jiang B, Ma Y (2017) Aging of zinc added to soils with a wide range of different properties: factors and modeling. Environ Toxicol Chem 36:2925–2933

    Article  CAS  Google Scholar 

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Acknowledgements

We thankfully acknowledged the received of Grant from DST-SERB (File No. EMR/2016/003761), Government of India for carrying out this research work. A support from DST-PURSE, University of Kalyani, is also highly acknowledged.

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Correspondence to Ekramul Islam.

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Bhakat, K., Chakraborty, A. & Islam, E. Characterization of zinc solubilization potential of arsenic tolerant Burkholderia spp. isolated from rice rhizospheric soil. World J Microbiol Biotechnol 37, 39 (2021). https://doi.org/10.1007/s11274-021-03003-8

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