Abstract
To study how biofilm-forming rhizobacteria isolated from mines and dumpsites improved the phytoremediation efficacy of B. juncea in metal-contaminated soil. Out of 91 isolates, six were chosen for research based on their tolerance to metals, and their efficient PGPR properties, and subjected to the design of a consortium. A compatibility study revealed no antagonistic interaction between rhizobacterial-consortiums. The results of the biofilm formation and FEG-SEM studies revealed that a consortium-BC8 formed a strong biofilm on the root surface of B. juncea seedlings. Based on results obtained with the phytoextraction efficiency of B. juncea in consortium-BC8 (SMHMZ46 and SMHMP23), they were identified as Klebsiella variicola and Pseudomonas otitidis, respectively, and submitted to NCBI GenBank with accession numbers MZ145092 and OK560623. This rhizobacteria is the first to be reported as assisting Ni and Pb phytoremediation by employing B. juncea. Soil inoculation with consortium-BC8 increased the amount of soluble Ni and Pb by 13.25-fold and 10.69-fold, respectively, when compared to the control. These consortiums-BC8 significantly increased vegetative growth and metal accumulation in root and shoot with a translocation-factor of 1.58 for Ni and soil to root with a bioconcentration-factor of 1.3 for Pb in B. juncea grown in individual soil contamination with 96.05 mg/kg NiCl2 and 89.63 mg/kg Pb(NO3)2, which are significantly higher than other consortium treatments and the non-inoculated control. B. juncea amendments with a biofilm-forming consortium-BC8 having TF, BCF, and BAC > 1 for Ni, whereas BCF > 1, TF, and BAC < 1 for Pb, are appropriate for green remediation of Ni and phytostabilization of Pb.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahmad I, Akhtar MJ, Asghar HN, Ghafoor U, Shahid M (2016) Differential effects of plant growth-promoting rhizobacteria on maize growth and cadmium uptake. J Plant Growth Regula 35(2):303–315. https://doi.org/10.1007/s00344-015-9534-5
Alaa FM (2018) Effectiveness of exopolysaccharides and biofilm forming plant growth promoting rhizobacteria on salinity tolerance of faba bean (Vicia faba L.). Afr J Microbiol Res 12(17):399–404. https://doi.org/10.5897/AJMR2018.8822
Ali A, Guo D, Li Y, Shaheen SM, Wahid F, Antoniadis V, Zhang Z (2021) Streptomyces pactum addition to contaminated mining soils improved soil quality and enhanced metals phytoextraction by wheat in a green remediation trial. Chemosphere 273:129692. https://doi.org/10.1016/j.chemosphere.2021.129692
Altaf MM, Ahmad I (2017) In vitro and in vivo biofilm formation by Azotobacter isolates and its relevance to rhizosphere colonization. Rhizosphere 3:138–142. https://doi.org/10.1016/j.rhisph.2017.04.009
Amin H, Arain BA, Jahangir TM, Abbasi MS, Amin F (2018) Accumulation and distribution of lead (Pb) in plant tissues of guar (Cyamopsis tetragonoloba L.) and sesame (Sesamum indicum L.): profitable phytoremediation with biofuel crops. Geol Ecol Landscapes 2(1):51–60. https://doi.org/10.1080/24749508.2018.1452464
Ansari FA, Ahmad I (2018) Biofilm development, plant growth promoting traits and rhizosphere colonization by Pseudomonas entomophila FAP1: a promising PGPR. Adv Microbiol 8(03):235. https://doi.org/10.4236/aim.2018.83016
Antoniadis V, Shaheen SM, Stärk HJ, Wennrich R, Levizou E, Merbach I, Rinklebe J (2021) Phytoremediation potential of twelve wild plant species for toxic elements in a contaminated soil. Environ Int 146:106233. https://doi.org/10.1016/j.envint.2020.106233
Arnow LE (1937) Colorimetric determination of the components of 3, 4-dihydroxyphenylalanine-tyrosine mixtures. J Biol Chem 118(2):531–537
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207. https://doi.org/10.1007/BF00018060
Castric PA (1975) Hydrogen cyanide, a secondary metabolite of Pseudomonas aeruginosa. Can J Microbiol 21(5):613–618. https://doi.org/10.1139/m75-088
Christensen GD, Simpson WA, Bisno AL, Beachey EH (1982) Adherence of slime-producing strains of Staphylococcus epidermidis to smooth surfaces. Infect Immun 37(1):318–326. https://doi.org/10.1128/iai.37.1.318-326.1982
Czaky T (1948) Estimation of bound hydroxylamine in biological materials. Acta Chem Scand 21:450–454. https://doi.org/10.3891/acta.chem.scand.02-0450
Din BU, Rafique M, Javed MT, Kamran MA, Mehmood S, Khan M, Chaudhary HJ (2020) Assisted phytoremediation of chromium spiked soils by Sesbania Sesban in association with Bacillus xiamenensis PM14: a biochemical analysis. Plant Physiol Biochem 146:249–258. https://doi.org/10.1016/j.plaphy.2019.11.010
Ekoa Bessa AZ, Ngueutchoua G, Kwewouo Janpou A, El-Amier YA, Njike Njome Mbella Nguetnga OA, Kankeu Kayou UR, Armstrong-Altrin JS (2021) Heavy metal contamination and its ecological risks in the beach sediments along the Atlantic Ocean (Limbe coastal fringes, Cameroon). Earth Syst Environ 5(2):433–444. https://doi.org/10.1007/s41748-020-00167-5
Farid M, Ali S, Akram NA, Rizwan M, Abbas F, Bukhari SAH, Saeed R (2017) Phyto-management of Cr-contaminated soils by sunflower hybrids: physiological and biochemical response and metal extractability under Cr stress. Environ Sci Pollut Res 24:16845–16859. https://doi.org/10.1007/s11356-017-9247-3
Fitz WJ, Wenzel WW (2002) Arsenic transformations in the soil–rhizosphere–plant system: fundamentals and potential application to phytoremediation. J Biotechnol 99(3):259–278. https://doi.org/10.1016/S0168-1656(02)00218-3
Freeman DJ, Falkiner FR, Keane CT (1989) New method for detecting slime production by coagulase negative staphylococci. J Clin Path 42(8):872–874. https://doi.org/10.1136/jcp.42.8.872
Goswami D, Vaghela H, Parmar S, Dhandhukia P, Thakker JN (2013) Plant growth promoting potentials of Pseudomonas spp. strain OG isolated from marine water. J Plant Interact 8(4):281–290. https://doi.org/10.1080/17429145.2013.768360
Halstead RL, Finn BJ, MacLean AJ (1969) Extractability of nickel added to soils and its concentration in plants. Can J Soil Sci 49(3):335–342. https://doi.org/10.4141/cjss69-046
Handa N, Kohli SK, Sharma A, Thukral AK, Bhardwaj R, Alyemeni MN, Ahmad P (2018) Selenium ameliorates chromium toxicity through modifications in pigment system, antioxidative capacity, osmotic system, and metal chelators in Brassica juncea seedlings. S Afr J Bot 119:1–10. https://doi.org/10.1016/j.sajb.2018.08.003
Hoque M, Hannan A, Imran S, Paul NC, Mondal M, Sadhin M, Rahman M, Bristi JM, Dola FS, Hanif M, Ye W, Brestic M, Rhaman MS (2022) Plant growth-promoting rhizobacteria-mediated adaptive responses of plants under salinity stress. J Plant Growth Regul 28:1–20. https://doi.org/10.1007/s00344-022-10633-1
IBM Corp. (2017) IBM SPSS Statistics for Windows. Armonk, NY: IBM Corp. Retrieved from https://hadoop.apache.org
Itusha A, Osborne WJ, Vaithilingam M (2019) Enhanced uptake of Cd by biofilm forming Cd resistant plant growth promoting bacteria bioaugmented to the rhizosphere of Vetiveria zizanioides. Int J Phytoreme 21(5):487–495. https://doi.org/10.1080/15226514.2018.1537245
Jeyasundar PGSA, Ali A, Azeem M, Li Y, Guo D, Sikdar A, Zhang Z (2021) Green remediation of toxic metals contaminated mining soil using bacterial consortium and Brassica juncea. Environ Pollut 277:116789. https://doi.org/10.1016/j.envpol.2021.116789
Jiang CY, Sheng XF, Qian M, Wang QY (2008) Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal-polluted soil. Chemosphere 72(2):157–164. https://doi.org/10.1016/j.chemosphere.2008.02.006
Kaur G, Asthir BJBP (2015) Proline: a key player in plant abiotic stress tolerance. Biol Plant 59:609–619. https://doi.org/10.1007/s10535-015-0549-3
Kaur R, Bhatti SS, Singh S, Singh J, Singh S (2018) Phytoremediation of heavy metals using cotton plant: a field analysis. Bull Environ Contam Toxicol 101(5):637–643. https://doi.org/10.1007/s00128-018-2472-8
Khanna K, Kohli SK, Ohri P, Bhardwaj R, Al-Huqail AA, Siddiqui MH, Ahmad P (2019) Microbial fortification improved photosynthetic efficiency and secondary metabolism in Lycopersicon esculentum plants under Cd stress. Biomolecules 9:581. https://doi.org/10.3390/biom9100581
Kushwaha A, Hans N, Kumar S, Rani R (2018) A critical review on speciation, mobilization and toxicity of lead in soil-microbe-plant system and bioremediation strategies. Ecotoxicol Environ Saf 147:1035–1045. https://doi.org/10.1016/j.ecoenv.2017.09.049
Lichtenthaler HK, Wellburn AR (1983) Determinations of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592
Lindsay WL, Norvell WA (1978) Development of a DTPA soil test for zinc, iron, manganese, and copper. Soil Sci Soc Am J 42:421–428. https://doi.org/10.2136/sssaj1978.03615995004200030009x
Ma Y, Rajkumar M, Rocha I, Oliveira RS, Freitas H (2015) Serpentine bacteria influence metal translocation and bioconcentration of Brassica juncea and Ricinus communis grown in multi-metal polluted soils. Front Plant Sci 5:757. https://doi.org/10.3389/fpls.2014.00757
Ma Y, Oliveira RS, Freitas H, Zhang C (2016) Biochemical and molecular mechanisms of plant-microbe-metal interactions: relevance for phytoremediation. Front Plant Sci 7:918. https://doi.org/10.3389/fpls.2016.00918
Mendoza-Hernández JC, Vázquez-Delgado OR, Castillo-Morales M, Varela-Caselis JL, Santamaría-Juárez JD, Olivares-Xometl O, Pérez-Osorio G (2019) Phytoremediation of mine tailings by Brassica juncea inoculated with plant growth-promoting bacteria. Microbiol Res 228:126308. https://doi.org/10.1016/j.micres.2019.126308
Mishra N, Sundari SK (2017) A `six-step-strategy’ to evaluate competence of plant growth promoting microbial consortia. Curr Sci 113(1):63–70
Ndeddy Aka RJ, Babalola OO (2016) Effect of bacterial inoculation of strains of Pseudomonas aeruginosa, Alcaligenes faecalis and Bacillus subtilis on germination, growth and heavy metal (Cd, Cr, and Ni) uptake of Brassica juncea. Int J Phytoreme 18(2):200–209. https://doi.org/10.1080/15226514.2015.1073671
Pikovskaya RI (1948) Mobilization of phosphorus in soil in connection with vital activity of some microbial species. Mikrobiologiya 17:362–370
Prajapati K, Prajapati M, Panchal R, Sharma S, Saraf MS (2022) Application of microorganisms for bioremediation of heavy metals. Acta Sci Environ Sci 1(1):01–09
Pramanik K, Mitra S, Sarkar A, Soren T, Maiti TK (2018) Characterization of a Cd2+-resistant plant growth promoting rhizobacterium (Enterobacter sp.) and its effects on rice seedling growth promotion under Cd2+-stress in vitro. Agric Nat Res 52(3):215–221. https://doi.org/10.1016/j.anres.2018.09.007
Rajkumar M, Freitas H (2008) Influence of metal resistant-plant growth-promoting bacteria on the growth of Ricinus communis in soil contaminated with heavy metals. Chemosphere 71(5):834–842. https://doi.org/10.1016/j.chemosphere.2007.11.038
Rajkumar M, Sandhya S, Prasad MNV, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30(6):1562–1574. https://doi.org/10.1016/j.biotechadv.2012.04.011
Reddy KR, Chinthamreddy S (2000) Comparison of extractants for removing heavy metals from contaminated clayey soils. J Soil Contam 9(5):449–462. https://doi.org/10.1080/10588330091134347
Rochlani A, Dalwani A, Shaikh NB, Shaikh N, Sharma S, Saraf MS (2022) Plant growth promoting rhizobacteria as biofertilizers: application in agricultural sustainability. Acta Sci Microbiol 5(4):12–21. https://doi.org/10.31080/ASMI.2022.05.1028
Rostami S, Azhdarpoor A (2019) The application of plant growth regulators to improve phytoremediation of contaminated soils: a review. Chemosphere 220:818–827. https://doi.org/10.1016/j.chemosphere.2018.12.203
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425. https://doi.org/10.1093/oxfordjournals.molbev.a040454
Saraf M, Sharma S, Thakkar A (2017) Production and optimization of siderophore from plant growth promoting Rhizobacteria. Braz J Microbiol 43:639–648
Schwyn B, Neilands JB (1987) Siderophores from agronomically important species of the Rhizobiacae. Comm Agric Food Chem 1(2):95–114
Shah RK and Saraf M (2019) Exploring inorganic phosphate solubilizing trait of halotolerant rhizobacteria isolated from Cuminum cyminum. Int J Res Advent Techno ISSN: 2321- 9637. http://ijrat.org/downloads/Vol-7/may-2019/752019107.pdf
Shaikh NB, Shaikh N, Rochlani A, Dalwani A, Sharma S, Saraf MS (2022) Rhizobacteria that promote plant growth and their impact on root system architecture, root development, and function. Acta Sci Microbiol 5(4):53–62. https://doi.org/10.31080/ASMI.2022.05.1035
Sharma P, Dubey RS (2005) Lead toxicity in plants. Braz J Plant Physiol 17:35–52
Sharma S, Saraf M (2022) Isolation, screening and biochemical characterizations with multiple traits of heavy metal tolerant rhizobacteria from mining area and landfill site. Adv Biores 13(1):147–156. https://doi.org/10.15515/abr.0976-4585.13.1.147156
Sharma S, Shah RK, Rathod ZR, Jain R, Lucie KM, Saraf M (2020) Isolation of heavy metal tolerant rhizobacteria from Zawar Mines Area, Udaipur, Rajasthan, India. Biosci Biotechnol Res Commu 13(1):233–238. https://doi.org/10.21786/bbrc/13.1specialissue/01
Sharma S, Rathod ZR, Saraf MS (2021) Elucidate the influence of heavy metal on bacterial growth isolated from a mining location and a waste dump: using their inducible mechanism. Curr Trends Biomedi Eng Biosci 20(2):001–006. https://doi.org/10.19080/CTBEB.2021.20.556034
Sharma S, Rathod ZR, Saraf MS (2022) Exploring the biotic stress tolerance potential of heavy metal tolerate rhizobacteria isolated from mines area and landfill site. Acta Sci Microbiol 5(2):31–37. https://doi.org/10.31080/ASMI.2022.05.1000
Sharma P, Bakshi P, Kaur R, Sharma A, Bhardwaj R, El-Sheikh MA, Ahmad P (2023a) Inoculation of plant-growth-promoting rhizobacteria and earthworms in the rhizosphere reinstates photosynthetic attributes and secondary metabolites in Brassica juncea L. under chromium toxicity. Plant Soil 483:573–587. https://doi.org/10.1007/s11104-022-05765-y
Sharma S, Rathod ZR, Jain R, Goswami D, Saraf M (2023b) Strategies to evaluate microbial consortia for mitigating abiotic stress in plants. Sustain Agrobiol Des Dev Microb Consort 43:177–203. https://doi.org/10.1007/978-981-19-9570-5_9
Sharma I (2020) Bioremediation techniques for polluted environment: concept, advantages, limitations, and prospects. In: Trace metals in the environment-new approaches and recent advances. IntechOpen pp. 221–235
Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enolo Viticult 16(3):144–158
Stepanović S, Vuković D, Hola V, Bonaventura GD, Djukić S, Ćirković I, Ruzicka F (2007) Quantification of biofilm in microtiter plates: overview of testing conditions and practical recommendations for assessment of biofilm production by staphylococci. APMIS 115(8):891–899. https://doi.org/10.1111/j.1600-0463.2007.apm_630.x
Sullivan TS, Gadd GM (2019) Metal bioavailability and the soil microbiome. Adv Agronomy 155:79–120. https://doi.org/10.1016/bs.agron.2019.01.004
Tank N, Saraf M (2009) Enhancement of plant growth and decontamination of nickel-spiked soil using PGPR. J Basic Microbiol 49(2):195–204. https://doi.org/10.1002/jobm.200800090
Wang Q, Shaheen SM, Jiang Y, Li R, Slaný M, Abdelrahman H, Zhang Z (2021) Fe/Mn-and P-modified drinking water treatment residuals reduced Cu and Pb phytoavailability and uptake in a mining soil. J Hazar Mater 403:123628. https://doi.org/10.1016/j.jhazmat.2020.123628
Wang Y, Huang W, Li Y, Yu F, Penttinen P (2022) Isolation, characterization, and evaluation of a high-siderophore-yielding bacterium from heavy metal–contaminated soil. Environ Sci Pollut Res 29(3):3888–3899. https://doi.org/10.1007/s11356-021-15996-8
Wuana RA, Okieimen FE, Imborvungu JA (2010) Removal of heavy metals from a contaminated soil using organic chelating acids. Int J Environ Sci Tech 7(3):485–496. https://doi.org/10.1007/BF03326158
Ying R, Xia B, Zeng X, Qiu R, Tang Y, Hu Z (2021) Adsorption of cadmium by Brassica juncea (L.) Czern. and Brassica pekinensis (Lour.) rupr in pot experiment. Sustainability 14(1):429. https://doi.org/10.3390/su14010429
Yu S, Teng C, Bai X, Liang J, Song T, Dong L, Qu J (2017) Optimization of siderophore production by Bacillus sp. PZ-1 and its potential enhancement of phytoextraction of Pb from soil. J Microbiol Biotechnol 27(8):1500–1512. https://doi.org/10.4014/jmb.1705.05021
Zaidi S, Usmani S, Singh BR, Musarrat J (2006) Significance of Bacillus subtilis strain SJ-101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica. Chemosphere 64(6):991–997. https://doi.org/10.1016/j.chemosphere.2005.12.057
Zainab N, Din BU, Javed MT, Afridi MS, Mukhtar T, Kamran MA, Chaudhary HJ (2020) Deciphering metal toxicity responses of flax (Linum usitatissimum L.) with exopolysaccharide and ACC-deaminase producing bacteria in industrially contaminated soils. Plant Physiol Biochem 152:90–99. https://doi.org/10.1016/j.plaphy.2020.04.039
Zhang X, Su C, Liu X, Liu Z, Liang X, Zhang Y, Feng Y (2020) Effect of plant-growth-promoting rhizobacteria on phytoremediation efficiency of Scirpus triqueter in pyrene-Ni co-contaminated soils. Chemosphere 241:125027. https://doi.org/10.1016/j.chemosphere.2019.125027
Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64(4):555–559. https://doi.org/10.1016/S0308-8146(98)00102-2
Acknowledgements
I am grateful to my guide for her support and encouragement, as well as the facilities offered by the DST-FIST-sponsored Department of Microbiology and Biotechnology, University School of Sciences, Gujarat University, Gujarat, India.
Funding
This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The writers have no beyond reconciliation circumstances in the arrangement of this material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Sharma, S., Saraf, M. Biofilm-forming plant growth-promoting rhizobacterial consortia isolated from mines and dumpsites assist green remediation of toxic metal (Ni and Pb) using Brassica juncea. BIOLOGIA FUTURA 74, 309–325 (2023). https://doi.org/10.1007/s42977-023-00179-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42977-023-00179-y