Effect of Pretreatments on bioremoval of metals and subsequent exposure to simulated gastrointestinal conditions
Main Article Content
Keywords
Adsorption, bioremediation, bioremoval, heavy metals, lactic acid bacteria
Abstract
Water contamination with heavy metals is increased due to environmental contaminants. Arsenic, cadmium, mercury, and lead are well-known toxic heavy metals for humans. Lactobacillus acidophilus is an ideal absorbent for the removal of metals from drinking water. In this study, the ability of treated and untreated L. acidophilus ATCC 4356 to remove four heavy metals, simultaneously, from multi-metallic contaminated water in 24 h was investigated. In addition, the stability of the bacteria–metal complexes was evaluated in simulated gastrointestinal tract conditions. According to the results, untreated L. acidophilus could remove 99.01% and 92.35% of mercury and lead in water, respectively (initial concentration of 700 µg.L−1; inoculum size of 2.6×1012 CFU.mL−1; pH 4; 37°C; 24 h), whereas removal of arsenic and cadmium, under the same conditions, was 91.28% and 61.91% by heat and NaOH treated cells, respectively. In the digest condition, the complexes of bacteria-metal were reversible and the bond stability of untreated bacteria–Hg complexes was stronger than other complexes. The results suggest that treated or untreated L. acidophilus ATCC 4356 cells have the potential to adsorb heavy metals in contaminated water.
References
Ameen, F.A., Hamdan, A.M. and El-Naggar, M.Y., 2020. Assessment of the heavy metal bioremediation efficiency of the novel marine lactic acid bacterium, Lactobacillus plantarum MF042018. Scientific Reports 10(1): 1–11. 10.1038/s41598-019-57210-3
Amiri, S., Mokarram, R.R., Khiabani, M.S., Bari, M.R., and Khaledabad, M.A., 2022. Characterization of antimicrobial peptides produced by Lactobacillus acidophilus LA-5 and Bifidobacterium lactis BB-12 and their inhibitory effect against foodborne pathogens. LWT 153: 112449. 10.1016/j.lwt.2021.112449
Amiri, S., Teymorlouei, M.J., Bari, M.R. and Khaledabad, M.A., 2021. Development of Lactobacillus acidophilus LA5-loaded whey protein isolate/lactose bionanocomposite powder by electrospraying: A strategy for entrapment. Food Bioscience 43: 101222. 10.1016/j.fbio.2021.101222
Asati, A., Pichhode, M. and Nikhil, K., 2016. Effect of heavy metals on plants: an overview. International Journal of Application or Innovation in Engineering & Management 5(3): 56–66.
Assi, M.A., Hezmee, M.N.M., Haron, A.W., Sabri, M.Y.M. and Rajion, M.A., 2016. The detrimental effects of lead on human and animal health. Veterinary World 9(6): 660. 10.14202/vetworld.2016.660-671
Bhakta, J., Ohnishi, K., Munekage, Y., Iwasaki, K. and Wei, M. 2012. Characterization of lactic acid bacteria-based probiotics as potential heavy metal sorbents. Journal of Applied Microbiology 112(6): 1193–1206. 10.1111/j.1365-2672.2012.05284.x
Bianchi, E., Biancalani, A., Berardi, C., Antal, A., Fibbi, D., Coppi, A., Lastrucci, L., Bussotti, N., Colzi, I. and Renai, L., 2020. Improving the efficiency of wastewater treatment plants: Bio-removal of heavy-metals and pharmaceuticals by Azolla filiculoides and Lemna minuta. Science of The Total Environment 746: 141219. 10.1016/j.scitotenv.2020.141219
Carocci, A., Rovito, N., Sinicropi, M.S. and Genchi, G., 2014. Mercury toxicity and neurodegenerative effects. In: Reviews of Environmental Contamination and Toxicology, Vol. 229. Springer, Cham, pp. 1–18. 10.1007/978-3-319-03777-6_1
Chen, Y., Zhang, B.-C., Sun, Y.-H., Zhang, J.-G., Sun, H.-J. and Wei, Z.-J., 2015. Physicochemical properties and adsorption of cholesterol by okra (Abelmoschus esculentus) powder. Food & Function 6(12): 3728–3736. 10.1039/C5FO00600G
Chen, Z., Pan, X., Chen, H., Guan, X. and Lin, Z., 2016. Biomineralization of Pb (II) into Pb-hydroxyapatite induced by Bacillus cereus 12-2 isolated from Lead–Zinc mine tailings. Journal of Hazardous Materials 301: 531–537. 10.1016/j.jhazmat.2015.09.023
Daisley, B.A., Monachese, M., Trinder, M., Bisanz, J.E., Chmiel, J.A., Burton, J.P. and Reid, G., 2019. Immobilization of cadmium and lead by Lactobacillus rhamnosus GR-1 mitigates apical-to-basolateral heavy metal translocation in a Caco-2 model of the intestinal epithelium. Gut Microbes 10(3): 321–333. 10.1080/19490976.2018.1526581
Dubinin, M., 1960. The potential theory of adsorption of gases and vapors for adsorbents with energetically nonuniform surfaces. Chemical Reviews 60(2): 235–241. 10.1021/cr60204a006
Elsanhoty, R.M., Salam, S.A., Ramadan, M.F. and Badr, F.H., 2014. Detoxification of aflatoxin M1 in yoghurt using probiotics and lactic acid bacteria. Food Control 43: 129–134. 10.1016/j.foodcont.2014.03.002
Fochesato, A.S., Cuello, D., Poloni, V., Galvagno, M.A., Dogi, C.A. and Cavaglieri, L.R., 2019. Aflatoxin B1 adsorption/desorption dynamics in the presence of Lactobacillus rhamnosus RC 007 in a gastrointestinal tract-simulated model. Journal of Applied Microbiology 126(1): 223–229. 10.1111/jam.14101
Freundlich, H., 1906. Uber die adsorption in losungen, zeitschrift fur phtsikalische chemie. Zeitschrift Fur Physikalische Chemie 62(5): 121–125.
Gerbino, E., Mobili, P., Tymczyszyn, E., Fausto, R. and GómezZavaglia, A., 2011. FTIR spectroscopy structural analysis of the interaction between Lactobacillus kefir S-layers and metal ions. Journal of Molecular Structure 987(1–3): 186–192. 10.1016/j.molstruc.2010.12.012
Göksungur, Y., Üren, S. and Güvenç, U., 2005. Biosorption of cadmium and lead ions by ethanol treated waste baker’s yeast biomass. Bioresource Technology 96(1): 103–109. 10.1016/j.biortech.2003.04.002
Hadiani, M.R., Khosravi-Darani, K. and Rahimifard, N., 2019. Optimization of As (III) and As (V) removal by Saccharomyces cerevisiae biomass for biosorption of critical levels in the food and water resources. Journal of Environmental Chemical Engineering 7(2): 102949. 10.1016/j.jece.2019.102949
Hadiani, M.R., Khosravi-Darani, K., Rahimifard, N. and Younesi, H., 2018. Assessment of mercury biosorption by Saccharomyces cerevisiae: response surface methodology for optimization of low Hg (II) concentrations. Journal of Environmental Chemical Engineering 6(4): 4980–4987. 10.1016/j.jece.2018.07.034
Kargar, S.H.M. and Shirazi, N.H., 2020. Lactobacillus fermentum and Lactobacillus plantarum bioremediation ability assessment for copper and zinc. Archives of Microbiology 202: 1957–1963. 10.1007/s00203-020-01916-w
Hsu, T.-C., Yi, P.-J., Lee, T.-Y. and Liu, J.-R., 2018. Probiotic characteristics and zearalenone-removal ability of a Bacillus licheniformis strain. PloS One 13(4): e0194866. 10.1371/journal.pone.0194866
Hussein, K.A., Hassan, S.H. and Joo, J.H., 2011. Potential capacity of Beauveria bassiana and Metarhizium anisopliae in the biosorption of Cd2+ and Pb2+. The Journal of General and Applied Microbiology 57(6): 347–355. 10.2323/jgam.57.347
Khosravi-Darani, K., Zoghi, A., Jazayeri, S. and da Cruz, A.G., 2020. Decontamination of aflatoxins with a focus on aflatoxin b1 by probiotic bacteria and yeasts: a review. Journal of Microbiology, Biotechnology and Food Sciences 10(3): 424–435. 10.15414/jmbfs.2020.10.3.424-435
Kirillova, A.V., Danilushkina, A.A., Irisov, D.S., Bruslik, N.L., Fakhrullin, R.F., Zakharov, Y.A., Bukhmin, V.S. and Yarullina, D.R., 2017. Assessment of resistance and bioremediation ability of Lactobacillus strains to lead and cadmium. International Journal of Microbiology 2017: 9869145. 10.1155/2017/9869145
Langmuir, I., 1918. The adsorption of gases on plane surfaces of glass, mica and platinum. Journal of the American Chemical Society 40(9): 1361–1403. 10.1021/ja02242a004
Lentini, P., Zanoli, L., Granata, A., Signorelli, S.S., Castellino, P. and Dell’Aquila, R., 2017. Kidney and heavy metals-The role of environmental exposure. Molecular Medicine Reports 15(5): 3413–3419. 10.3892/mmr.2017.6389
Li, X., Ming, Q., Cai, R., Yue, T., Yuan, Y., Gao, Z. and Wang, Z., 2020. Biosorption of Cd2+ and Pb2+ from apple juice by the magnetic nanoparticles functionalized lactic acid bacteria cells. Food Control 109: 106916. 10.1016/j.foodcont.2019.106916
Li, Z., Ma, Z., van der Kuijp, T.J., Yuan, Z. and Huang, L., 2014. A review of soil heavy metal pollution from mines in China: pollution and health risk assessment. Science of the Total Environment 468: 843–853. 10.1016/j.scitotenv.2013.08.090
Maham, M., Karami-Osboo, R., Kiarostami, V. and Waqif-Husain, S., 2013. Novel binary solvents-dispersive liquid—liquid micro-extraction (BS-DLLME) method for determination of patulin in apple juice using high-performance liquid chromatography. Food Analytical Methods 6(3): 761–766. 10.1007/s12161-012-9483-6
Massoud, R., Khosravi-Darani, K., Sharifan, A., Asadi, G. and Hadiani, M., 2020. Mercury Biodecontamination from Milk by using L. acidophilus ATCC 4356. Journal of Pure Applied Microbiology 14(4): 2313–2321. 10.22207/JPAM.14.4.10
Massoud, R., Khosravi-Darani, K., Sharifan, A., Asadi, G. and Zoghi, A., 2020. Lead and cadmium biosorption from milk by Lactobacillus acidophilus ATCC 4356. Food Science & Nutrition 8(10): 5284–5291. 10.1002/fsn3.1825
Medina-Pizzali, M., Damián-Bastidas, N. and Vargas-Reyes, M., 2019. Arsenic in baby foods: health effects and dietary exposure. Quality Assurance and Safety of Crops & Foods 11(4): 369–380. 10.3920/QAS2018.1477
Mirmahdi, R.S., Mofid, V., Zoghi, A., Khosravi_Darani, K. and Mortazavian, A.M., 2022. Risk of low stability Saccharomyces cerevisiae ATCC 9763-heavy metals complex in gastrointestinal simulated conditions. Heliyon 8: e09452. 10.1016/j.heliyon.2022.e09452
Mirmahdi, R.S., Zoghi, A., Mohammadi, F., Khosravi-Darani, K., Jazaiery, S., Mohammadi, R. and Rehman, Y., 2021. Biodecontamination of milk and dairy products by probiotics: Boon for bane. Italian Journal of Food Science 33(SP1): 78–91. 10.15586/ijfs.v33iSP2.2053
Moghaddam, S.T., Javadi, A. and Matin, A.A., 2020. Reduction of bisphenol A by Lactobacillus acidophilus and Lactobacillus plantarum in yoghurt. International Journal of Dairy Technology 73(4): 737–742. 10.1111/1471-0307.12706
Moghari, A.A., Razavi, S., Ehsani, M., Mousavi, M., and Nia, T.H., 2015. Chemical, proteolysis and sensory attributes, and probiotic microorganisms viability of Iranian ultrafiltered-Feta cheese as a function of inulin concentration and storage temperature. Quality Assurance and Safety of Crops & Foods 7(2): 217–224. 10.3920/QAS2013.0326
Monachese, M., Burton, J.P. and Reid, G., 2012. Bioremediation and tolerance of humans to heavy metals through microbial processes: a potential role for probiotics? Applied and Environmental Microbiology 78(18): 6397. 10.1128/AEM.01665-12
Musawi, A.M., Johari, W.L.W., Ikhsan, N.F.M., Ahmad, S.A., Yasid, N.A. and Shukor, M.Y., 2019. The growth potential and bioaccumulation ability of probiotics under the exposure of different heavy metals. Pertanika Journal of Tropical Agricultural Science 42(1): 305–314. http://www.pertanika.upm.edu.my/
Pan, J., Ge, X., Liu, R. and Tang, H., 2006. Characteristic features of Bacillus cereus cell surfaces with biosorption of Pb (II) ions by AFM and FT-IR. Colloids and surfaces B: Biointerfaces 52(1): 89–95. 10.1016/j.colsurfb.2006.05.016
Pandey, G. and Madhuri, S., 2014. Heavy metals causing toxicity in animals and fishes. Research Journal of Animal, Veterinary and Fishery Sciences 2(2): 17–23. https://www.researchgate.net/publication/270169412
Park, J.-D. and Zheng, W., 2012. Human exposure and health effects of inorganic and elemental mercury. Journal of Preventive Medicine and Public Health 45(6): 344. 10.3961/jpmph.2012.45.6.344
Perczak, A., Goliński, P., Bryła, M. and Waśkiewicz, A., 2018. The efficiency of lactic acid bacteria against pathogenic fungi and mycotoxins. Arhiv za higijenu rada i toksikologiju 69(1): 32–44. 10.2478/aiht-2018-69-3051
Petruzzi, L., Corbo, M.R., Sinigaglia, M. and Bevilacqua, A., 2016. Ochratoxin A removal by yeasts after exposure to simulated human gastrointestinal conditions. Journal of Food Science 81(11): M2756–M2760. 10.1111/1750-3841.13518
Prasad, K.S., Ramanathan, A., Paul, J., Subramanian, V. and Prasad, R., 2013. Biosorption of arsenite (As+3) and arsenate (As+5) from aqueous solution by Arthrobacter sp. biomass. Environmental Technology 34(19): 2701–2708. 10.1080/09593330.2013.786137
Ryan, J., Hutchings, S.C., Fang, Z., Bandara, N., Gamlath, S., Ajlouni, S. and Ranadheera, C.S., 2020. Microbial, physico-chemical and sensory characteristics of mango juice-enriched probiotic dairy drinks. International Journal of Dairy Technology 73(1): 182–190. 10.1111/1471-0307.12630
Sharma, H., Rawal, N. and Mathew, B.B., 2015. The characteristics, toxicity and effects of cadmium. International Journal of Nanotechnology and Nanoscience 3: 1–9.
Sieuwerts, S., De Bok, F.A., Mols, E., De Vos, W.M. and Vlieg, J.H., 2008. A simple and fast method for determining colony forming units. Letters in Applied Microbiology 47(4): 275–278. 10.1111/j.1472-765X.2008.02417.x
Sohrabpour, S., Bari, M.R., Alizadeh, M. and Amiri, S., 2021. Investigation of the rheological, microbial, and physico-chemical properties of developed synbiotic yogurt containing Lactobacillus acidophilus LA-5, honey, and cinnamon extract. Journal of Food Processing and Preservation 45(4): e15323. 10.1111/jfpp.15323
Teemu, H., Seppo, S., Jussi, M., Raija, T. and Kalle, L., 2008. Reversible surface binding of cadmium and lead by lactic acid and bifidobacteria. International Journal of Food Microbiology 125(2): 170–175. 10.1016/j.ijfoodmicro.2008.03.041
Tempkin, M. and Pyzhev, V., 1940. Kinetics of ammonia synthesis on promoted iron catalyst. Acta Physico-Chimica Sinica USSR 12(1): 327.
Teodorowicz, M., Van Neerven, J. and Savelkoul, H., 2017. Food processing: The influence of the maillard reaction on immunogenicity and allergenicity of food proteins. Nutrients 9(8): 835. 10.3390/nu9080835
Thirunavukkarasu, O., Viraraghavan, T., Subramanian, K. and Tanjore, S., 2002. Organic arsenic removal from drinking water. Urban Water 4(4): 415–421. 10.1016/S1462-0758(02)00029-8
Tunali, S., Akar, T., Özcan, A.S., Kiran, I. and Özcan, A., 2006. Equilibrium and kinetics of biosorption of lead (II) from aqueous solutions by Cephalosporium aphidicola. Separation and Purification Technology 47(3): 105–112. 10.1016/j.seppur.2005.06.009
Wang, L., Wang, Z., Yuan, Y., Cai, R., Niu, C., and Yue, T., 2015. Identification of key factors involved in the biosorption of patulin by inactivated lactic acid bacteria (LAB) cells. PloS One 10(11): e0143431. 10.1371/journal.pone.0143431
World Health Organization. 2006. Guidelines for drinking-water quality: incorporating first addendum. Vol. 1, Recommendations, third (ed.). World Health Organization.
Yin, J., Wu, B., Liu, S., Hu, S., Gong, T., Cherr, G.N., Zhang, X.-X., Ren, H., and Xian, Q., 2018. Rapid and complete dehalogenation of halonitromethanes in simulated gastrointestinal tract and its influence on toxicity. Chemosphere 211: 1147–1155. 10.1016/j.chemosphere.2018.08.039
Zhai, Q., Wang, G., Zhao, J., Liu, X., Narbad, A., Chen, Y.Q., Zhang, H., Tian, F. and Chen, W., 2014. Protective effects of Lactobacillus plantarum CCFM8610 against chronic cadmium toxicity in mice indicate routes of protection besides intestinal sequestration. Applied and Environmental Microbiology 80(13): 4063–4071. 10.1128/AEM.00762-14
Zhai, Q., Yin, R., Yu, L., Wang, G., Tian, F., Yu, R., Zhao, J., Liu, X., Chen, Y.Q., and Zhang, H., 2015. Screening of lactic acid bacteria with potential protective effects against cadmium toxicity. Food Control 54: 23–30. 10.1016/j.foodcont.2015.01.037
Zhao, L., Jin, H., Lan, J., Zhang, R., Ren, H., Zhang, X. and Yu, G., 2015. Detoxification of zearalenone by three strains of Lactobacillus plantarum from fermented food in vitro. Food Control 54: 158–164. 10.1016/j.foodcont.2015.02.003
Zoghi, A., Khosravi-Darani, K. and Sohrabvandi, S., 2014. Surface binding of toxins and heavy metals by probiotics. Mini Reviews in Medicinal Chemistry 14(1): 84–98. 10.2174/1389557513666131211105554
Zoghi, A., Khosravi _Darani, K. and Hekmatdoost, A., 2021. Effects of pretreatments on patulin removal from apple juices using lactobacilli: binding stability in simulated gastrointestinal condition and modeling. Probiotics and Antimicrobial Proteins 13(1): 135–145. 10.1007/s12602-020-09666-3
Zoghi, A., Massoud, R., Todorov, S.D., Chikindas, M.L., Popov, I., Smith, S. and Khosravi-Darani, K., (2021). Role of the lactobacilli in food bio-decontamination: Friends with benefits. Enzyme and Microbial Technology 150: 109861. 10.1016/j.enzmictec.2021.109861