Abstract
Purpose
Due to the inevitable interaction between bacteria and soil minerals, whether bacteria could exert the excepted functions in the soil is yet to be confirmed and how minerals affect biosorption potential is needed to be investigated. The purposes of this study were to explore the adsorption behavior and mechanism of metal-resistant bacteria attaching to typical red soil minerals under different conditions and to discuss whether biosorption potential would be altered after the addition of functional bacteria to soil.
Materials and methods
Here, we tested equilibrium adsorption along with zeta potential analysis, scanning electron microscopy (SEM), Fourier transform infrared spectra (FTIR), and desorption to investigate the adsorption of two metal-resistant bacteria (Gram-negative Enterobacter sp. EG16 and Gram-positive Bacillus subtilis DBM) onto typical red soil minerals including goethite, kaolinite, and gibbsite under different environmental factors.
Results and discussion
We found that the minerals adsorbed more EG16 cells than DBM, and the adsorption capacities followed the sequence of goethite > kaolinite > gibbsite. Both the surfaces of bacteria and mineral were pH-dependent in our tested pH range (4.0–7.0), and the maximum adsorption was at pH 4.0. Increasing ionic strength resulted in less adsorption of bacteria onto goethite, whereas bacterial adsorption onto kaolinite was the opposite. These observations elucidated that electrostatic interaction was the dominant contributor. The adsorption conformed to the Langmuir and pseudo-second-order kinetic model implying chemical adsorption, and the result of FTIR also supported that. Desorption experiment has suggested the significant contribution of electrostatic force and the minor dominator of functional groups for bacteria–mineral combination.
Conclusions
The results of this study indicated that electrostatic interaction was the dominant contributor to bacteria–mineral combination and functional groups coordination contributed less than 10%. This finding suggested most adhered bacteria could still provide active sites for heavy metal biosorption. Thus, although 50–90% of added functional bacteria has adhered to minerals, the bacteria–mineral combination had a limited impact on biosorption.
Graphical abstract
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ams DA, Fein JB, Dong H, Maurice PA (2004) Experimental measurements of the adsorption of Bacillus subtilis and Pseudomonas mendocina onto Fe-oxyhydroxide-coated and uncoated quartz grains. Geomicrobiol J 21:511–519. https://doi.org/10.1080/01490450490888172
Bai J, Yang X, Du R, Chen Y, Wang S, Qiu R (2014) Biosorption mechanisms involved in immobilization of soil Pb by Bacillus subtilis DBM in a multi-metal-contaminated soil. J Environ Sci (China) 26:2056–2064. https://doi.org/10.1016/j.jes.2014.07.015
Belimov AA, Hontzeas N, Safronova VI, Demchinskaya SV, Piluzza G, Bullitta S, Glick BR (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37:241–250. https://doi.org/10.1016/j.soilbio.2004.07.033
Beveridge TJ (1981) Ultrastructure, chemistry, and function of the bacterial wall. Int Rev Cytol 72:229–317. https://doi.org/10.1016/s0074-7696(08)61198-5
Cai P, Huang Q, Walker SL (2013) Deposition and survival of Escherichia coli O157:H7 on clay minerals in a parallel plate flow system. Environ Sci Technol 47:1896–1903. https://doi.org/10.1021/es304686a
Cao Y, Wei X, Cai P, Huang Q, Rong X, Liang W (2011) Preferential adsorption of extracellular polymeric substances from bacteria on clay minerals and iron oxide. Colloids Surf B Biointerfaces 83:122–127. https://doi.org/10.1016/j.colsurfb.2010.11.018
Chatterjee S, Sau GB, Mukherjee SK (2009) Plant growth promotion by a hexavalent chromium reducing bacterial strain, Cellulosimicrobium cellulans KUCr3. World J Microbiol Biotechnol 25:1829–1836. https://doi.org/10.1007/s11274-009-0084-5
Chen Y et al (2016a) Survival strategies of the plant-associated bacterium Enterobacter sp. strain EG16 under cadmium stress. Appl Environ Microbiol 82:1734–1744. https://doi.org/10.1128/AEM.03689-15
Chen Y, Yang W, Chao Y, Wang S, Tang Y-T, Qiu R-L (2016b) Metal-tolerant Enterobacter sp. strain EG16 enhanced phytoremediation using Hibiscus cannabinus via siderophore-mediated plant growth promotion under metal contamination. Plant Soil 413:203–216. https://doi.org/10.1007/s11104-016-3091-y
Cheng PF, Wang Y, Cheng K, Li FB, Qin HL, Liu TX (2017) The acid base buffer capacity of red soil variable charge minerals and its surface complexation model. Acta Chim Sinica 75:637–644. https://doi.org/10.6023/A17020056
Das SK, Guha AK (2007) Biosorption of chromium by Termitomyces clypeatus. Colloids Surf B Biointerfaces 60:46–54 https://doi.org/10.1016/j.colsurfb.2007.05.021
Doshi H, Ray A, Kothari IL (2007) Biosorption of cadmium by live and dead Spirulina: IR spectroscopic, kinetics, and SEM studies. Curr Microbiol 54:213–218. https://doi.org/10.1007/s00284-006-0340-y
Dursun AY (2006) A comparative study on determination of the equilibrium, kinetic and thermodynamic parameters of biosorption of copper(II) and lead(II) ions onto pretreated Aspergillus niger. Biochem Eng J 28:187–195. https://doi.org/10.1016/j.bej.2005.11.003
Eren E, Afsin B (2008) An investigation of cu(II) adsorption by raw and acid-activated bentonite: a combined potentiometric, thermodynamic, XRD, IR, DTA study. J Hazard Mater 151:682–691. https://doi.org/10.1016/j.jhazmat.2007.06.040
Fang L, Cai P, Chen W, Liang W, Hong Z, Huang Q (2009) Impact of cell wall structure on the behavior of bacterial cells in the binding of copper and cadmium. Colloids Surf Physicochem Eng Aspects 347:50–55. https://doi.org/10.1016/j.colsurfa.2008.11.041
Fang L et al (2011) Binding characteristics of copper and cadmium by cyanobacterium Spirulina platensis. J Hazard Mater 190:810–815. https://doi.org/10.1016/j.jhazmat.2011.03.122
Hermansson M (1999) The DLVO theory in microbial adhesion. Colloids Surf B Biointerfaces 14:105–119. https://doi.org/10.1016/s0927-7765(99)00029-6
Hong ZN, Zhao G, Chen WL, Rong XM, Cai P, Dai K, Huang QY (2014) Effects of solution chemistry on bacterial adhesion with phyllosilicates and goethite explained by the extended DLVO theory. Geomicrobiol J 31:419–430. https://doi.org/10.1080/01490451.2013.824523
Hong ZN, Jiang J, Li JY, Xu RK (2018) Preferential adhesion of surface groups of Bacillus subtilis on gibbsite at different ionic strengths and pHs revealed by ATR-FTIR spectroscopy. Colloids Surf B Biointerfaces 165:83–91. https://doi.org/10.1016/j.colsurfb.2018.02.020
Jiang D, Huang Q, Cai P, Rong X, Chen W (2007) Adsorption of Pseudomonas putida on clay minerals and iron oxide. Colloids Surf B Biointerfaces 54:217–221. https://doi.org/10.1016/j.colsurfb.2006.10.030
Joshi PM, Juwarkar AA (2009) In vivo studies to elucidate the role of extracellular polymeric substances from Azotobacter in immobilization of heavy metals. Environ Sci Technol 43:5884–5889. https://doi.org/10.1021/es900063b
Juwarkar AA, Nair A, Dubey KV, Singh SK, Devotta S (2007) Biosurfactant technology for remediation of cadmium and lead contaminated soils. Chemosphere 68:1996–2002. https://doi.org/10.1016/j.chemosphere.2007.02.027
Kulczycki E, Ferris FG, Fortin D (2002) Impact of cell wall structure on the behavior of bacterial cells as sorbents of cadmium and lead. Geomicrobiol J 19:553–565. https://doi.org/10.1080/01490450290098586
Kulczycki E, Fowle DA, Fortin D, Ferris FG (2005) Sorption of cadmium and lead by bacteria–ferrihydrite composites. Geomicrobiol J 22:299–310. https://doi.org/10.1080/01490450500184694
Liu CC et al (2010) Mineral magnetism to probe into the nature of palaeomagnetic signals of subtropical red soil sequences in southern. China GeoJI 181:1395–1410. https://doi.org/10.1111/j.1365-246X.2010.04592.x
Liu LJ, Xu FY, Yu ZL, Dong P (2012) Facile fabrication of non-sticking superhydrophobic boehmite film on Al foil. Appl Surf Sci 258:8928–8933. https://doi.org/10.1016/j.apsusc.2012.05.119
Loukidou MX, Zouboulis AI, Karapantsios TD, Matis KA (2004) Equilibrium and kinetic modeling of chromium(VI) biosorption by Aeromonas caviae. Colloids Surf Physicochem Eng Aspects 242:93–104. https://doi.org/10.1016/j.colsurfa.2004.03.030
Lu Y et al (2015) Impacts of soil and water pollution on food safety and health risks in China. Environ Int 77:5–15. https://doi.org/10.1016/j.envint.2014.12.010
Luo SL et al (2011) Analysis and characterization of cultivable heavy metal-resistant bacterial endophytes isolated from Cd-hyperaccumulator Solanum nigrum L. and their potential use for phytoremediation. Chemosphere 85:1130–1138. https://doi.org/10.1016/j.chemosphere.2011.07.053
Ma Y, Rajkumar M, Luo YM, Freitas H (2011) Inoculation of endophytic bacteria on host and non-host plants--effects on plant growth and Ni uptake. J Hazard Mater 195:230–237. https://doi.org/10.1016/j.jhazmat.2011.08.034
Moon EM, Peacock CL (2013) Modelling Cu(II) adsorption to ferrihydrite and ferrihydrite-bacteria composites: deviation from additive adsorption in the composite sorption system. Geochim Cosmochim Acta 104:148–164. https://doi.org/10.1016/j.gca.2012.11.030
Nath J, Ray L (2015) Biosorption of Malachite green from aqueous solution by dry cells of Bacillus cereus M-16(1) (MTCC 5521). J Environ Chem Eng 3:386–394. https://doi.org/10.1016/j.jece.2014.12.022
Ngwenya BT, Sutherland IW, Kennedy L (2003) Comparison of the acid-base behaviour and metal adsorption characteristics of a gram-negative bacterium with other strains. Appl Geochem 18:527–538. https://doi.org/10.1016/S0883-2927(02)00118-X
Poorebrahimi S, Norouzbeigi R (2015) A facile solution-immersion process for the fabrication of superhydrophobic gibbsite films with a binary micro-nano structure: effective factors optimization via Taguchi method. Appl Surf Sci 356:157–166. https://doi.org/10.1016/j.apsusc.2015.07.172
Rajkumar M, Sandhya S, Prasad MN, Freitas H (2012) Perspectives of plant-associated microbes in heavy metal phytoremediation. Biotechnol Adv 30:1562–1574. https://doi.org/10.1016/j.biotechadv.2012.04.011
Rong X, Huang Q, He X, Chen H, Cai P, Liang W (2008) Interaction of Pseudomonas putida with kaolinite and montmorillonite: a combination study by equilibrium adsorption, ITC, SEM and FTIR. Colloids Surf B Biointerfaces 64:49–55. https://doi.org/10.1016/j.colsurfb.2008.01.008
Rong X, Chen W, Huang Q, Cai P, Liang W (2010) Pseudomonas putida adhesion to goethite: studied by equilibrium adsorption, SEM, FTIR and ITC. Colloids Surf B Biointerfaces 80:79–85. https://doi.org/10.1016/j.colsurfb.2010.05.037
Ruan HD, Frost RL, Kloprogge JT (2001) The behavior of hydroxyl units of synthetic goethite and its dehydroxylated product hematite. Spectrochim Acta A Mol Biomol Spectrosc 57:2575–2586. https://doi.org/10.1016/s1386-1425(01)00445-0
Saikia NJ, Bharali DJ, Sengupta P, Bordoloi D, Goswamee RL, Saikia PC, Borthakur PC (2003) Characterization, beneficiation and utilization of a kaolinite clay from Assam, India. Appl Clay Sci 24:93–103. https://doi.org/10.1016/S0169-1317(03)00151-0
Santhiya D, Subramanian S, Natarajan KA (2001) Surface chemical studies on sphalerite and galena using Bacillus polymyxa. J Colloid Interface Sci 235:298–309. https://doi.org/10.1006/jcis.2000.7256
Sinha S, Mukherjee SK (2008) Cadmium-induced siderophore production by a high Cd-resistant bacterial strain relieved Cd toxicity in plants through root colonization. Curr Microbiol 56:55–60. https://doi.org/10.1007/s00284-007-9038-z
Turgay OC, Bilen S (2012) The role of plant growth-promoting rhizosphere bacteria in toxic metal extraction by Brassica spp. https://doi.org/10.1007/978-94-007-3913-0_8
Ueshima M, Ginn BR, Haack EA, Szymailowski JES, Fein FB (2008) Cd adsorption onto Pseudomonas putida in the presence and absence of extracellular polymeric substances. Geochim Cosmochim Acta 72:5885–5895. https://doi.org/10.1016/j.gca.2008.09.014
Vivas A, Biro B, Ruiz-Lozano JM, Barea JM, Azcon R (2006) Two bacterial strains isolated from a Zn-polluted soil enhance plant growth and mycorrhizal efficiency under Zn-toxicity. Chemosphere 62:1523–1533. https://doi.org/10.1016/j.chemosphere.2005.06.053
Wang Q, Xiong D, Zhao P, Yu X, Tu B, Wang G (2011) Effect of applying an arsenic-resistant and plant growth-promoting rhizobacterium to enhance soil arsenic phytoremediation by Populus deltoides LH05-17. J Appl Microbiol 111:1065–1074. https://doi.org/10.1111/j.1365-2672.2011.05142.x
Wang N, Du HH, Huang QY, Cai P, Rong XM, Feng XH, Chen WL (2016) Surface complexation modeling of Cd(II) sorption to montmorillonite, bacteria, and their composite. Biogeosciences 13:5557–5566. https://doi.org/10.5194/bg-13-5557-2016
Wang L, Ji B, Hu Y, Liu R, Sun W (2017) A review on in situ phytoremediation of mine tailings. Chemosphere 184:594–600. https://doi.org/10.1016/j.chemosphere.2017.06.025
Wilson MJ (1994) Clay mineralogy: spectroscopic and chemical determinative methods. 10.1007/978-94-011-0727-3
Yee N, Fein JB, Daughney CJ (2000) Experimental study of the pH, ionic strength, and reversibility behavior of bacteria-mineral adsorption. Geochim Cosmochim Acta 64:609–617. https://doi.org/10.1016/S0016-7037(99)00342-7
Yuan P, Annabi-Bergaya F, Tao Q, Fan M, Liu Z, Zhu J, He H, Chen T (2008) A combined study by XRD, FTIR, TG and HRTEM on the structure of delaminated Fe-intercalated/pillared clay. J Colloid Interface Sci 324:142–149. https://doi.org/10.1016/j.jcis.2008.04.076
Zeng F, Ali S, Zhang H, Ouyang Y, Qiu B, Wu F, Zhang G (2011) The influence of pH and organic matter content in paddy soil on heavy metal availability and their uptake by rice plants. Environ Pollut 159:84–91. https://doi.org/10.1016/j.envpol.2010.09.019
Zhang TX, Yang WH, Zhu XY, Wang HZ, Brookes PC, Xu J (2014) The pH dependence of Escherichia coli O157:H7 adsorption on kaolinite and goethite surfaces. J Soils Sediments 15:106–116. https://doi.org/10.1007/s11368-014-0948-7
Zhao WQ, Liu X, Huang QY, Walker SL, Cai P (2012) Interactions of pathogens Escherichia coli and Streptococcus suis with clay minerals. Appl Clay Sci 69:37–42. https://doi.org/10.1016/j.clay.2012.07.003
Acknowledgments
The authors are grateful to the reviewers who help us improve the paper by many pertinent comments and suggestions.
Funding
This work was supported by the National Key Research and Development Program (2018YFD0800700), the Youth Program of National Natural Science Foundation of China (41807031), Natural Science Foundation of Guangdong Province (2018A030310127), and China Postdoctoral Science Foundation Funded Project (2018M643309).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible editor: Yuan Ge
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
ESM 1
(PDF 435 kb)
Rights and permissions
About this article
Cite this article
Feng, W., Li, Y., Lin, Z. et al. The influence on biosorption potentials of metal-resistant bacteria Enterobacter sp. EG16 and Bacillus subtilis DBM by typical red soil minerals. J Soils Sediments 20, 3217–3229 (2020). https://doi.org/10.1007/s11368-020-02650-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11368-020-02650-y