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In Vitro Evaluation of Bioremediation Capacity of a Commercial Probiotic, Bacillus clausii, for Chromium (VI) and Lead (II) Toxicity
Abstract
Heavy metals cause disastrous effects on any living organisms. Probiotics have the ability to reduce metal toxicity. Commercial probiotics having bioremediation capacity can use these bacteria as an alternative to conventional remediation methods. The bioaccumulation of heavy metals including chromium (VI) (Cr [VI]) and lead (II) (Pb [II]) causes fatal toxicity in humans. Some naturally occurring bacterial species, such as Bacillus and Pseudomonas, contribute their role in bioremediation of these heavy metals and also some of the species of Bacillus are proven probiotics. However, there is no study conducted on Bacillus clausii, which is a proven probiotic species of genus Bacillus.
The aim of this study was to isolate and characterize heavy metals that are resistant probiotics. Probiotic containing B. clausii was grown overnight at 37°C in Luria-Bertani (HiMedia, M1245) medium. Morphological, biochemical, and probiotic characterization was performed using probiotic culture followed by a preliminary heavy metal minimum inhibitory concentration (MIC) test. Moreover, the plates prepared having a two-fold concentration ranging 1–600 ppm of potassium dichromate and lead acetate as Cr and Pb source, demonstrated good probiotic characteristics at 525 ppm were able to tolerate both Pb and Cr and showed the highest level of Pb and Cr removal from the inoculated medium.
Keywords: Bacillus clausii, bioaccumulation, bioremediation, Enterogermina, probiotics
REFERENCES
[1] Radwan MA, Salama AK. Market basket survey for some heavy metals in Egyptian fruits and vegetables. Food Chem Toxicol. 2006; 44: 1273–1278p.
[2] Tuzen M, Soylak M. Evaluation of trace element contents in canned foods marketed from Turkey. Food Chem. 2007; 102: 1089–1095p.
[3] Duran A, Tuzen M, Soylak M. Trace element levels in some dried fruit samples from Turkey. Int J Food Sci Nutr. 2008; 59: 581–589p.
[4] Wang S, Shi X. Molecular mechanisms of metal toxicity and carcinogenesis. Mol Cell Biochem. 2001; 222: 3–9p.
[5] In: LW Chang, L Magos, T Suzuki, editor. Toxicology of Metals. Boca Raton, FL, USA: CRC Press; 1996.
[6] Beyersmann D, Hartwig A. Carcinogenic metal compounds: Recent insight into molecular and cellular mechanisms. Arch Toxicol. 2008; 82 (8): 493–512p.
[7] Yedjou CG, Tchounwou PB. Oxidative stress in human leukemia (HL-60), human liver carcinoma (HepG2), and human (Jurkat-T) cells exposed to arsenic trioxide. Metal Ions Biol Med. 2006; 9: 298–303p.
[8] Yedjou GC, Tchounwou PB. In-vitro cytotoxic and genotoxic effects of arsenic trioxide on human leukemia (HL-60) cells using the MTT and alkaline single cell gel electrophoresis (Comet) assays. Mol Cell Biochem. 2007; 301: 123–130p.
[9] Tchounwou PB, Centeno JA, Patlolla AK. Arsenic toxicity, mutagenesis, and carcinogenesis – A health risk assessment and management approach. Mol Cell Biochem. 2004; 255: 47–55p.
[10] Tchounwou PB, Ishaque A, Schneider J. Cytotoxicity and transcriptional activation of stress genes in human liver carcinoma cells (HepG2) exposed to cadmium chloride. Mol Cell Biochem. 2001; 222: 21–28p.
[11] Patlolla AK, Barnes C, Hackett D, Tchounwou PB. Potassium dichromate induced cytotoxicity, genotoxicity and oxidative stress in human liver carcinoma (HepG2) cells. Int J Environ Res Public Health. 2009; 6: 643–653p.
[12] Patlolla AK, Barnes C, Yedjou C, Velma VR, Tchounwou PB. Oxidative stress, DNA damage, and antioxidant enzyme activity induced by hexavalent chromium in Sprague-Dawley rats. Environ Toxicol. 2009; 24 (1): 66–73p.
[13] Yedjou CG, Tchounwou PB. N-acetyl-l-cysteine affords protection against lead-induced cytotoxicity and oxidative stress in human liver carcinoma (HepG2) cells. Int J Environ Res Public Health. 2008; 4 (2): 132–137p.
[14] Tchounwou PB, Yedjou CG, Foxx DN, Ishaque AB, Shen E. Lead-induced cytotoxicity and transcriptional activation of stress genes in human liver carcinoma (HepG2) cells. Mol Cell Biochem. 2004; 255: 161–170p.
[15] Sutton DJ, Tchounwou PB. Mercury induces the externalization of phosphatidyl-serine in human renal proximal tubule (HK-2) cells. Int J Environ Res Public Health. 2007; 4 (2): 138–144p.
[16] Sutton DJ, Tchounwou PB, Ninashvili N, Shen E. Mercury induces cytotoxicity and transcriptionally activates stress genes in human liver carcinoma (HepG2) cells. Int J Mol Sci. 2002; 3 (9): 965–984p.
[17] Bartlett RJ. Chromium cycling in soils and water: Links, gaps, and methods. Environ Health Perspect. 1991; 92: 17–24p.
[18] Bhakta JN, Ohnishi K, Munekage Y, Iwasaki K. Isolation and probiotic characterization of arsenic‑resistant lactic acid bacteria for uptaking arsenic. Int J Chem Biol Eng. 2010; 4: 831–838p.
[19] Bhakta JN, Ohnishi K, Munekage Y, Iwasaki K, Wei MQ. Characterization of lactic acid bacteria‑based probiotics as potential heavy metal sorbents. J Appl Microbiol. 2012; 112: 1193–1206p.
[20] Wu JJ, Du RP, Gao M, Sui YQ, Xiu L, Wang X. Naturally occurring lactic acid bacteria isolated from tomato pomace silage. Asian‑Australas J Anim Sci. 2014; 27: 648–657p.
[21] Abbas S, Ahmed I, Kudo T, Iida T, Ali GM, Fujiwara T, et al. Heavy metal‑tolerant and psychrotolerant bacterium Acinetobacter pakistanensis sp. nov., isolated from a textile dyeing wastewater treatment pond. Pak J Agric Sci. 2014; 51: 595–608p.
[22] Abbas S, Ahmed I, Iida T, Lee YJ, Busse HJ, Fujiwara T, et al. A heavy‑metal tolerant novel bacterium, Alcaligenes pakistanensis sp. nov., isolated from industrial effluent in Pakistan. Antonie Van Leeuwenhoek. 2015; 108: 859–870p.
[23] Beveridge TJ, Murray RG. Sites of metal deposition in the cell wall of Bacillus subtilis. J Bacteriol. 1980; 141: 876–887p.
[24] Beveridge TJ, Koval SF. Binding of metals to cell envelopes of Escherichia coli K‑12. Appl Environ Microbiol. 1981; 42: 325–335p.
[25] Mowll JL, Gadd GM. Cadmium uptake by Aureobasidium pullulans. J Gen Microbiol. 1984; 130: 279–284p.
[26] Beveridge TJ, Fyfe WS. Metal fixation by bacterial cell walls. Can J Earth Sci. 1985; 22: 1893–1898p.
[27] Hamlett NV, Landale EC, Davis BH, Summers AO. Roles of the Tn21 merT, merP, and merC gene products in mercury resistance and mercury binding. J Bacteriol. 1992; 174: 6377–6385p.
[28] Carlin A, Shi W, Dey S, Rosen BP. The ars operon of Escherichia coli confers arsenical and antimonial resistance. J Bacteriol. 1995; 177: 981–986p.
[29] Silver S. Bacterial resistances to toxic metal ions – A review. Gene. 1996; 179: 9–19p.
[30] Valls M, Gonzalez‑Duarte R, Atrian S, De Lorenzo V. Bioaccumulation of heavy metals with protein fusions of metallothionein to bacterial OMPs. Biochimie. 1998; 80: 855–861p.
[31] White C, Gadd GM. Accumulation and effects of cadmium on sulphate‑reducing bacterial biofilms. Microbiology. 1998; 144: 1407–1415p.
[32] Sayler GS, Ripp S. Field applications of genetically engineered microorganisms for bioremediation processes. Curr Opin Biotechnol. 2000; 11: 286–289p.
[33] Fein JB, Martin AM, Wightman PG. Metal adsorption onto bacterial surfaces: Development of a predictive approach. Geochim Cosmochim Acta. 2001; 65: 4267–4273p.
[34] Das N, Vimala R, Karthika P. Biosorption of heavy metals: An overview. Indian J Biotechnol. 2008; 7: 159–169p.
[35] Wang J, Li Q, Li MM, Chen TH, Zhou YF, Yue ZB. Competitive adsorption of heavy metal by extracellular polymeric substances (EPS) extracted from sulfate reducing bacteria. Bioresour Technol. 2014; 163: 374–376p.
[36] Rosca M, Hlihor RM, Cozma P, Comanita ED, Simion IM, Gavrilescu M. Potential of biosorption and bioaccumulation processes for heavy metals removal in bioreactors. In: Proceedings of the 2015 E‑Health and Bioengineering Conference (EHB). IEEE. 2015.
[37] Todar K. The Good, the Bad, and the Deadly. 1st edition. WY, USA: Opalescent Pool in Yellowstone National Park; 2004.
[38] Nielsen P, Fritze D, Priest FG. Phenetic diversity of alkaliphilic Bacillus strains: Proposal for nine new species. Microbiology. 1995; 141: 1745–1761p.
[39] Arihara K, Ota H, Itoh M, Kondo Y, Sameshima T, Yamanaka H, et al. Lactobacillus acidophilus group lactic acid bacteria applied to meat fermentation. J Food Sci. 1998; 63: 544–547p.
[40] Fortina MG, Parini C, Rossi P, Manachini PL. Mapping of three plasmids from Lactobacillus helveticus ATCC 15009. Lett Appl Microbiol. 1993; 17: 303–306p.
[41] Sheeladevi A, Ramanathan N. Lactic acid production using lactic acid bacteria under optimized conditions. Int J Pharm Biol Arch. 2012; 2: 1681–1691p.
[42] Nwanyanwu CE, Abu GO. Influence of growth media on hydrophobicity of phenol-utilizing bacteria found in petroleum refinery effluent. Int Res J Biol Sci. 2013; 2: 6–10p.
[43] APHA. Standard Methods for the Examination of Water and Wastewater. 18th edition. Washington, DC, USA: APHA; 1989.
[44] Fifield FW, Haines PJ. Environmental Analytical Chemistry. 2nd edition. London, UK: Blackwell Science; 2000.
[45] CPCB. Guide Manual: Water and Wastewater Analysis. India: Ministry of Water Resources; 2011. pp. 164–166.
[46] da Costa ACA, Duta FP. Bioaccumulation of copper, zinc, cadmium and lead by Bacillus sp., Bacillus cereus, Bacillus sphaericus and Bacillus subtilis. Braz J Microbiol. 2001; 32: 1–6p.
[47] Khatun M, Bera P, Mitra D, Mandal A, Samanta A. Estimation of heavy metal tolerance and antibiotic susceptibility of Bacillus cereus isolated from municipal solid waste. Int J Pharma Bio Sci. 2012; 3: 819–829p.
[48] Mols M, Abee T. Bacillus cereus responses to acid stress. Environ Microbiol. 2011; 13: 2835–2843p.
[49] Strompfova V, Laukova A. In vitro study on bacteriocin production of Enterococci associated with chickens. Anaerobe. 2007; 13: 228–237p.
[50] Cebeci A, Gurakan C. Properties of potential probiotic Lactobacillus plantarum strains. Food Microbiol. 2003; 20: 511–518p.
[51] Maldonado NC, de Ruiz CS, Nader-Macias ME. Design of a beneficial product for newborn calves by combining Lactobacilli, minerals, and vitamins. Prep Biochem Biotechnol. 2015; 46: 648–656p.
[52] Allameh SK, Ringø E, Yusoff FM, Daud HM, Ideris A. Properties of Enterococcus faecalis, a new probiotic bacterium isolated from the intestine of snakehead fish (Channa striatus Bloch). Afr J Microbiol Res. 2014; 8: 2215–2222p.
[53] Tavakoli M, Hamidi-Esfahani Z, Hejazi MA, et al. Characterization of probiotic abilities of Lactobacilli isolated from Iranian Koozeh traditional cheese. Pol J Food Nutr Sci. 2017; 67: 41–48p.
[54] Adami A, Cavazzoni V. Occurrence of selected bacterial groups in the faeces of piglets fed with Bacillus coagulans as probiotic. J Basic Microbiol. 1999; 39: 3–9p.
[55] Basu M, Bhattacharya S, Paul AK. Isolation and characterization of chromium‑resistant bacteria from tannery effluents. Bull Environ Contam Toxicol. 1997; 58: 535–542p.
[56] Kamala‑Kannan S, Lee KJ. Metal tolerance and antibiotic resistance of Bacillus species isolated from Sunchon Bay sediments, South Korea. Biotechnology. 2008; 7: 149–152p.
[57] Matyar F, Kaya A, Dinçer S. Antibacterial agents and heavy metal resistance in Gram‑negative bacteria isolated from seawater, shrimp and sediment in Iskenderun Bay, Turkey. Sci Total Environ. 2008; 407: 279–285p.
[58] Khusro A, Preetam Raj JP, Panicker SG, et al. Multiple heavy metals response and antibiotic sensitivity pattern of Bacillus subtilis strain KPA. J Chem Pharm Res. 2014; 6: 532–538p.
[59] Mishra R, Sinha V, Kannan A, Upreti RK. Reduction of chromium‑VI by chromium resistant lactobacilli: A prospective bacterium for bioremediation. Toxicol Int. 2012; 19: 25–30p.
[60] Angkau P. Comparative Lactic Acid Production Between Enterococcus faecalis and Enterococcus faecium in Hydrolysed Sago Starch. Malaysia: Universiti Malaysia Sarawak; 2013.
[61] Jung MY, Kim JS, Chang YH. Bacillus acidiproducens sp. nov., vineyard soil isolates that produce lactic acid. Int J Syst Evol Microbiol. 2017; 59: 2226–2231p.
[62] Kaczorek E, Chrzanowski Ł, Pijanowska A, Olszanowski A. Yeast and bacteria cell hydrophobicity and hydrocarbon biodegradation in the presence of natural surfactants: Rhamnolipides and saponins. Bioresour Technol. 2008; 99: 4285–4291p.
[63] Obuekwe CO, Al-Jadi ZK, Al-Saleh ES. Hydrocarbon degradation in relation to cell-surface hydrophobicity among bacterial hydrocarbon degraders from petroleum-contaminated Kuwait desert environment. Int Biodeterior Biodegr. 2009; 63: 273–279p.
[64] Torres S, Pandey A, Castro GR. Organic solvent adaptation of Gram positive bacteria: Applications and biotechnological potentials. Biotechnol Adv. 2011; 29: 442–452p.
[65] Ianeva OD. [Mechanisms of bacteria resistance to heavy metals]. Mikrobiol Z. 2009; 71: 54–65p.
The aim of this study was to isolate and characterize heavy metals that are resistant probiotics. Probiotic containing B. clausii was grown overnight at 37°C in Luria-Bertani (HiMedia, M1245) medium. Morphological, biochemical, and probiotic characterization was performed using probiotic culture followed by a preliminary heavy metal minimum inhibitory concentration (MIC) test. Moreover, the plates prepared having a two-fold concentration ranging 1–600 ppm of potassium dichromate and lead acetate as Cr and Pb source, demonstrated good probiotic characteristics at 525 ppm were able to tolerate both Pb and Cr and showed the highest level of Pb and Cr removal from the inoculated medium.
Keywords: Bacillus clausii, bioaccumulation, bioremediation, Enterogermina, probiotics
REFERENCES
[1] Radwan MA, Salama AK. Market basket survey for some heavy metals in Egyptian fruits and vegetables. Food Chem Toxicol. 2006; 44: 1273–1278p.
[2] Tuzen M, Soylak M. Evaluation of trace element contents in canned foods marketed from Turkey. Food Chem. 2007; 102: 1089–1095p.
[3] Duran A, Tuzen M, Soylak M. Trace element levels in some dried fruit samples from Turkey. Int J Food Sci Nutr. 2008; 59: 581–589p.
[4] Wang S, Shi X. Molecular mechanisms of metal toxicity and carcinogenesis. Mol Cell Biochem. 2001; 222: 3–9p.
[5] In: LW Chang, L Magos, T Suzuki, editor. Toxicology of Metals. Boca Raton, FL, USA: CRC Press; 1996.
[6] Beyersmann D, Hartwig A. Carcinogenic metal compounds: Recent insight into molecular and cellular mechanisms. Arch Toxicol. 2008; 82 (8): 493–512p.
[7] Yedjou CG, Tchounwou PB. Oxidative stress in human leukemia (HL-60), human liver carcinoma (HepG2), and human (Jurkat-T) cells exposed to arsenic trioxide. Metal Ions Biol Med. 2006; 9: 298–303p.
[8] Yedjou GC, Tchounwou PB. In-vitro cytotoxic and genotoxic effects of arsenic trioxide on human leukemia (HL-60) cells using the MTT and alkaline single cell gel electrophoresis (Comet) assays. Mol Cell Biochem. 2007; 301: 123–130p.
[9] Tchounwou PB, Centeno JA, Patlolla AK. Arsenic toxicity, mutagenesis, and carcinogenesis – A health risk assessment and management approach. Mol Cell Biochem. 2004; 255: 47–55p.
[10] Tchounwou PB, Ishaque A, Schneider J. Cytotoxicity and transcriptional activation of stress genes in human liver carcinoma cells (HepG2) exposed to cadmium chloride. Mol Cell Biochem. 2001; 222: 21–28p.
[11] Patlolla AK, Barnes C, Hackett D, Tchounwou PB. Potassium dichromate induced cytotoxicity, genotoxicity and oxidative stress in human liver carcinoma (HepG2) cells. Int J Environ Res Public Health. 2009; 6: 643–653p.
[12] Patlolla AK, Barnes C, Yedjou C, Velma VR, Tchounwou PB. Oxidative stress, DNA damage, and antioxidant enzyme activity induced by hexavalent chromium in Sprague-Dawley rats. Environ Toxicol. 2009; 24 (1): 66–73p.
[13] Yedjou CG, Tchounwou PB. N-acetyl-l-cysteine affords protection against lead-induced cytotoxicity and oxidative stress in human liver carcinoma (HepG2) cells. Int J Environ Res Public Health. 2008; 4 (2): 132–137p.
[14] Tchounwou PB, Yedjou CG, Foxx DN, Ishaque AB, Shen E. Lead-induced cytotoxicity and transcriptional activation of stress genes in human liver carcinoma (HepG2) cells. Mol Cell Biochem. 2004; 255: 161–170p.
[15] Sutton DJ, Tchounwou PB. Mercury induces the externalization of phosphatidyl-serine in human renal proximal tubule (HK-2) cells. Int J Environ Res Public Health. 2007; 4 (2): 138–144p.
[16] Sutton DJ, Tchounwou PB, Ninashvili N, Shen E. Mercury induces cytotoxicity and transcriptionally activates stress genes in human liver carcinoma (HepG2) cells. Int J Mol Sci. 2002; 3 (9): 965–984p.
[17] Bartlett RJ. Chromium cycling in soils and water: Links, gaps, and methods. Environ Health Perspect. 1991; 92: 17–24p.
[18] Bhakta JN, Ohnishi K, Munekage Y, Iwasaki K. Isolation and probiotic characterization of arsenic‑resistant lactic acid bacteria for uptaking arsenic. Int J Chem Biol Eng. 2010; 4: 831–838p.
[19] Bhakta JN, Ohnishi K, Munekage Y, Iwasaki K, Wei MQ. Characterization of lactic acid bacteria‑based probiotics as potential heavy metal sorbents. J Appl Microbiol. 2012; 112: 1193–1206p.
[20] Wu JJ, Du RP, Gao M, Sui YQ, Xiu L, Wang X. Naturally occurring lactic acid bacteria isolated from tomato pomace silage. Asian‑Australas J Anim Sci. 2014; 27: 648–657p.
[21] Abbas S, Ahmed I, Kudo T, Iida T, Ali GM, Fujiwara T, et al. Heavy metal‑tolerant and psychrotolerant bacterium Acinetobacter pakistanensis sp. nov., isolated from a textile dyeing wastewater treatment pond. Pak J Agric Sci. 2014; 51: 595–608p.
[22] Abbas S, Ahmed I, Iida T, Lee YJ, Busse HJ, Fujiwara T, et al. A heavy‑metal tolerant novel bacterium, Alcaligenes pakistanensis sp. nov., isolated from industrial effluent in Pakistan. Antonie Van Leeuwenhoek. 2015; 108: 859–870p.
[23] Beveridge TJ, Murray RG. Sites of metal deposition in the cell wall of Bacillus subtilis. J Bacteriol. 1980; 141: 876–887p.
[24] Beveridge TJ, Koval SF. Binding of metals to cell envelopes of Escherichia coli K‑12. Appl Environ Microbiol. 1981; 42: 325–335p.
[25] Mowll JL, Gadd GM. Cadmium uptake by Aureobasidium pullulans. J Gen Microbiol. 1984; 130: 279–284p.
[26] Beveridge TJ, Fyfe WS. Metal fixation by bacterial cell walls. Can J Earth Sci. 1985; 22: 1893–1898p.
[27] Hamlett NV, Landale EC, Davis BH, Summers AO. Roles of the Tn21 merT, merP, and merC gene products in mercury resistance and mercury binding. J Bacteriol. 1992; 174: 6377–6385p.
[28] Carlin A, Shi W, Dey S, Rosen BP. The ars operon of Escherichia coli confers arsenical and antimonial resistance. J Bacteriol. 1995; 177: 981–986p.
[29] Silver S. Bacterial resistances to toxic metal ions – A review. Gene. 1996; 179: 9–19p.
[30] Valls M, Gonzalez‑Duarte R, Atrian S, De Lorenzo V. Bioaccumulation of heavy metals with protein fusions of metallothionein to bacterial OMPs. Biochimie. 1998; 80: 855–861p.
[31] White C, Gadd GM. Accumulation and effects of cadmium on sulphate‑reducing bacterial biofilms. Microbiology. 1998; 144: 1407–1415p.
[32] Sayler GS, Ripp S. Field applications of genetically engineered microorganisms for bioremediation processes. Curr Opin Biotechnol. 2000; 11: 286–289p.
[33] Fein JB, Martin AM, Wightman PG. Metal adsorption onto bacterial surfaces: Development of a predictive approach. Geochim Cosmochim Acta. 2001; 65: 4267–4273p.
[34] Das N, Vimala R, Karthika P. Biosorption of heavy metals: An overview. Indian J Biotechnol. 2008; 7: 159–169p.
[35] Wang J, Li Q, Li MM, Chen TH, Zhou YF, Yue ZB. Competitive adsorption of heavy metal by extracellular polymeric substances (EPS) extracted from sulfate reducing bacteria. Bioresour Technol. 2014; 163: 374–376p.
[36] Rosca M, Hlihor RM, Cozma P, Comanita ED, Simion IM, Gavrilescu M. Potential of biosorption and bioaccumulation processes for heavy metals removal in bioreactors. In: Proceedings of the 2015 E‑Health and Bioengineering Conference (EHB). IEEE. 2015.
[37] Todar K. The Good, the Bad, and the Deadly. 1st edition. WY, USA: Opalescent Pool in Yellowstone National Park; 2004.
[38] Nielsen P, Fritze D, Priest FG. Phenetic diversity of alkaliphilic Bacillus strains: Proposal for nine new species. Microbiology. 1995; 141: 1745–1761p.
[39] Arihara K, Ota H, Itoh M, Kondo Y, Sameshima T, Yamanaka H, et al. Lactobacillus acidophilus group lactic acid bacteria applied to meat fermentation. J Food Sci. 1998; 63: 544–547p.
[40] Fortina MG, Parini C, Rossi P, Manachini PL. Mapping of three plasmids from Lactobacillus helveticus ATCC 15009. Lett Appl Microbiol. 1993; 17: 303–306p.
[41] Sheeladevi A, Ramanathan N. Lactic acid production using lactic acid bacteria under optimized conditions. Int J Pharm Biol Arch. 2012; 2: 1681–1691p.
[42] Nwanyanwu CE, Abu GO. Influence of growth media on hydrophobicity of phenol-utilizing bacteria found in petroleum refinery effluent. Int Res J Biol Sci. 2013; 2: 6–10p.
[43] APHA. Standard Methods for the Examination of Water and Wastewater. 18th edition. Washington, DC, USA: APHA; 1989.
[44] Fifield FW, Haines PJ. Environmental Analytical Chemistry. 2nd edition. London, UK: Blackwell Science; 2000.
[45] CPCB. Guide Manual: Water and Wastewater Analysis. India: Ministry of Water Resources; 2011. pp. 164–166.
[46] da Costa ACA, Duta FP. Bioaccumulation of copper, zinc, cadmium and lead by Bacillus sp., Bacillus cereus, Bacillus sphaericus and Bacillus subtilis. Braz J Microbiol. 2001; 32: 1–6p.
[47] Khatun M, Bera P, Mitra D, Mandal A, Samanta A. Estimation of heavy metal tolerance and antibiotic susceptibility of Bacillus cereus isolated from municipal solid waste. Int J Pharma Bio Sci. 2012; 3: 819–829p.
[48] Mols M, Abee T. Bacillus cereus responses to acid stress. Environ Microbiol. 2011; 13: 2835–2843p.
[49] Strompfova V, Laukova A. In vitro study on bacteriocin production of Enterococci associated with chickens. Anaerobe. 2007; 13: 228–237p.
[50] Cebeci A, Gurakan C. Properties of potential probiotic Lactobacillus plantarum strains. Food Microbiol. 2003; 20: 511–518p.
[51] Maldonado NC, de Ruiz CS, Nader-Macias ME. Design of a beneficial product for newborn calves by combining Lactobacilli, minerals, and vitamins. Prep Biochem Biotechnol. 2015; 46: 648–656p.
[52] Allameh SK, Ringø E, Yusoff FM, Daud HM, Ideris A. Properties of Enterococcus faecalis, a new probiotic bacterium isolated from the intestine of snakehead fish (Channa striatus Bloch). Afr J Microbiol Res. 2014; 8: 2215–2222p.
[53] Tavakoli M, Hamidi-Esfahani Z, Hejazi MA, et al. Characterization of probiotic abilities of Lactobacilli isolated from Iranian Koozeh traditional cheese. Pol J Food Nutr Sci. 2017; 67: 41–48p.
[54] Adami A, Cavazzoni V. Occurrence of selected bacterial groups in the faeces of piglets fed with Bacillus coagulans as probiotic. J Basic Microbiol. 1999; 39: 3–9p.
[55] Basu M, Bhattacharya S, Paul AK. Isolation and characterization of chromium‑resistant bacteria from tannery effluents. Bull Environ Contam Toxicol. 1997; 58: 535–542p.
[56] Kamala‑Kannan S, Lee KJ. Metal tolerance and antibiotic resistance of Bacillus species isolated from Sunchon Bay sediments, South Korea. Biotechnology. 2008; 7: 149–152p.
[57] Matyar F, Kaya A, Dinçer S. Antibacterial agents and heavy metal resistance in Gram‑negative bacteria isolated from seawater, shrimp and sediment in Iskenderun Bay, Turkey. Sci Total Environ. 2008; 407: 279–285p.
[58] Khusro A, Preetam Raj JP, Panicker SG, et al. Multiple heavy metals response and antibiotic sensitivity pattern of Bacillus subtilis strain KPA. J Chem Pharm Res. 2014; 6: 532–538p.
[59] Mishra R, Sinha V, Kannan A, Upreti RK. Reduction of chromium‑VI by chromium resistant lactobacilli: A prospective bacterium for bioremediation. Toxicol Int. 2012; 19: 25–30p.
[60] Angkau P. Comparative Lactic Acid Production Between Enterococcus faecalis and Enterococcus faecium in Hydrolysed Sago Starch. Malaysia: Universiti Malaysia Sarawak; 2013.
[61] Jung MY, Kim JS, Chang YH. Bacillus acidiproducens sp. nov., vineyard soil isolates that produce lactic acid. Int J Syst Evol Microbiol. 2017; 59: 2226–2231p.
[62] Kaczorek E, Chrzanowski Ł, Pijanowska A, Olszanowski A. Yeast and bacteria cell hydrophobicity and hydrocarbon biodegradation in the presence of natural surfactants: Rhamnolipides and saponins. Bioresour Technol. 2008; 99: 4285–4291p.
[63] Obuekwe CO, Al-Jadi ZK, Al-Saleh ES. Hydrocarbon degradation in relation to cell-surface hydrophobicity among bacterial hydrocarbon degraders from petroleum-contaminated Kuwait desert environment. Int Biodeterior Biodegr. 2009; 63: 273–279p.
[64] Torres S, Pandey A, Castro GR. Organic solvent adaptation of Gram positive bacteria: Applications and biotechnological potentials. Biotechnol Adv. 2011; 29: 442–452p.
[65] Ianeva OD. [Mechanisms of bacteria resistance to heavy metals]. Mikrobiol Z. 2009; 71: 54–65p.
DOI: https://doi.org/10.37628/jibb.v4i2.340
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