Skip to main content
SpringerLink
Log in

Successive use of microorganisms to remove chromium from wastewater

  • Mini-Review
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Heavy metal pollution is a direct consequence of the extensive utilization of heavy metals in various industrial processes. The persistence and nondegradability of heavy metals cause them to bioaccumulate in nature, and when they come in direct contact with the pristine environment, they not only contaminate it severely but also pose dire consequences to the health of all living forms on earth, including humans. Chromium (Cr) is one of the heavy metals which has been extensively used in various industrial processes such as mining, alloy manufacturing, tanning of hides and skins, pigment production, etc. However, it is regarded as a priority pollutant due to its highly toxic, teratogenic, mutagenic, and carcinogenic nature, and the U.S. Environmental Protection Agency (EPA) also categorized it into group “A” human carcinogen. In contrast to water-soluble hexavalent chromium (Cr6+), its reduced form, trivalent chromium (Cr3+), is relatively benign and readily precipitated at environmental pH. Thus, bioremediation of Cr6+ through microorganisms including bacteria, yeast, and algae provides a promising approach to decontaminate a metal-polluted environment. This review describes an overview of the microbial reduction of Cr6+, resistance mechanism, and the antioxidant profiling exhibited by these microorganisms when exposed to Cr6+. It also describes the pilot-scale study of the successive use of bacterial, fungal, and algal strains and the subsequent use of microbially purified water for the cultivation of plant growth. Multiple metal-resistant microorganisms are a good bioresource for green chemistry to eradicate environmental Cr6+.

Key Points

• Hexavalent chromium (Cr 6+ ) is highly toxic for living organisms including humans.

• Microbial Cr resistance is mediated at the genetic, proteomic, and molecular levels.

• Successive use of microorganisms is the best strategy to exterminate Cr 6+ from the environment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ackerley DF, Gonzalez CF, Park CH, Blake R II, Keyhan M, Matin A (2004) Chromate-reducing properties of soluble flavoproteins from Pseudomonas putida and Escherichia coli. Appl Environ Microbiol 70(2):873–882

    PubMed  PubMed Central  CAS  Google Scholar 

  • Ackerley DF, Barak Y, Lynch SV, Curtin J, Matin A (2006) Effect of chromate stress on Escherichia coli K-12. J Bacteriol 188:3371–3381

    PubMed  PubMed Central  CAS  Google Scholar 

  • Akcil A, Erust C, Ozdemiroglu S, Fonti V, Beolchini F (2015) A review of approaches and techniques used in aquatic contaminated sediments: metal removal and stabilization by chemical and biotechnological processes. J Clean Prod 86:24–36

    CAS  Google Scholar 

  • Al-Asheh S, Duvnjak Z (1995) Adsorption of copper and chromium by Aspergillus carbonarius. Biotechnol Prog 11:638–642

    PubMed  CAS  Google Scholar 

  • Alvarez AH, Moreno-Sanchez R, Cervantes C (1999) Chromate efflux by means of the ChrA chromate resistance protein from Pseudomonas aeruginosa. J Bacteriol 181:7398–7400

    PubMed  PubMed Central  CAS  Google Scholar 

  • Amatussalam A, Abubacker MN, Rajendran RB (2011) In situ Carica papaya stem matrix and Fusarium oxysporum (NCBT-156) mediated bioremediation of chromium. Indian J Exp Biol 49:925–931

    PubMed  CAS  Google Scholar 

  • An Z, Zhang H, Wen Q, Chen Z, Du M (2014) Desalination combined with hexavalent chromium reduction in a microbial desalination cell. Desalination 354:181–188

    CAS  Google Scholar 

  • Anand P, Isar J, Saran S, Saxena RK (2006) Bioaccumulation of copper by Trichoderma viride. Bioresour Technol 97(8):1018–1025

    PubMed  CAS  Google Scholar 

  • Appenroth KJ, Bischoff MB, Gabrys H, Stoeckel J, Swartz HM, Walczak T, Winnefeld K (2000) Kinetics of chromium (V) formation and reduction in fronds of the duckweed Spirodela polyrhiza—a low frequency EPR study. J Inorg Biochem 78:235–242

    PubMed  CAS  Google Scholar 

  • Ayangbenro AS, Babalola O (2017) A new strategy for heavy metal polluted environments: a review of microbial biosorbents. Int J Environ Res Public Health 14:94

    PubMed Central  Google Scholar 

  • Bagchi D, Bagchi M, Stohs SJ (2001) Chromium (VI)-induced oxidative stress, apoptotic cell death and modulation of p53 tumor suppressor gene. Mol Cell Biochem 222:149–158

    PubMed  CAS  Google Scholar 

  • Bagchi D, Stohs SJ, Downs BW, Bagchi M, Preuss HG (2002) Cytotoxicity and oxidative mechanisms of different forms of chromium. Toxicology 180:5–22

    PubMed  CAS  Google Scholar 

  • Bai J, Wu X, Fan F, Tian W, Yin X, Zhao L, Fan F, Li Z, Tian L, Qin Z, Guo J (2012) Biosorption of uranium by magnetically modified Rhodotorula glutinis. Enzym Microb Technol 51(6):382–387

    CAS  Google Scholar 

  • Barnhart J (1997) Occurrence, uses and properties of chromium. Regul Toxicol Pharmacol 26:S3–S7

    PubMed  CAS  Google Scholar 

  • Barrera-Díaz CE, Lugo-Lugo V, Bilyeu B (2012) A review of chemical, electrochemical and biological methods for aqueous Cr(VI) reduction. J Hazard Mater 1(12):223–224

    Google Scholar 

  • Baruthio F (1992) Toxic effects of chromium and its compounds. Biol Trace Elem Res 32:145–153

    PubMed  CAS  Google Scholar 

  • Batool R, Yrjala K, Hasnain S (2012) Hexavalent chromium reduction by bacteria from tannery effluent. J Microbiol Biotechnol 22(4):547–554

    PubMed  CAS  Google Scholar 

  • Biedermann KA, Landolph JR (1990) Role of valence state and solubility of chromium compounds on induction of cytotoxicity, mutagenesis, and anchorage independence in diploid human fibroblasts. Cancer Res 50:7835–7842

    PubMed  CAS  Google Scholar 

  • Bielicka-Giełdoń A, Bojanowska I, Wiśniewski A (2005) Two faces of chromium—pollutant and bioelement. Pol J Environ Stud 14(1):5–10

    Google Scholar 

  • Bopp LH, Erlich HL (1988) Chromate resistance and reduction in Pseudomonas fluorescens strain LB300. Arch Microbiol 150:426–431

    CAS  Google Scholar 

  • Bopp LH, Chakrabarty AM, Ehrlich HL (1983) Chromate resistance plasmid in Pseudomonas fluorescens. J Bacteriol 155:1105–1109

    PubMed  PubMed Central  CAS  Google Scholar 

  • Borges KM, Boswell JS, Liebross RH, Wetterhahn KE (1991) Activation of chromium (VI) by thiols results in chromium (V) formation, chromium binding to DNA and altered DNA conformation. Carcinogenesis 12(4):551–561

    PubMed  CAS  Google Scholar 

  • Brady D, Letebele B, Duncan JR, Rose PD (1994) Bioaccumulation of metals by Scenedesmus, Selenastrum and Chlorella algae. Water SA 20:213–218

    CAS  Google Scholar 

  • Branco R, Chung AP, Johnston T, Gurel V, Morais P, Zhitkovich A (2008) The chromate-inducible chrBACF operon from the transposable element TnOtChr confers resistance to chromium (VI) and superoxide. J Bacteriol 190:6996–7003

    PubMed  PubMed Central  CAS  Google Scholar 

  • Calder LM (1988) Chromium contamination of groundwater. In: Niagru JO, Nieboer NE (eds) Chromium in natural and human environments. Wiley Interscience, New York, pp 215–231

    Google Scholar 

  • Cárdenas-González JF, Acosta-Rodríguez I (2010) Hexavalent chromium removal by a Paecilomyces sp fungal strain isolated from environment. Bioinorg Chem Appl 2010

  • Cefalu WT, Frank BH (2004) Role of chromium in human health and in diabetes. Diabetes Care 27:2741–2751

    PubMed  CAS  Google Scholar 

  • Cervantes C, Ohtake H (1988) Plasmid-determined resistance to chromate in Pseudomonas aeruginosa. FEMS Microbiol Lett 56:173–176

    CAS  Google Scholar 

  • Cervantes C, Ohtake H, Chu L, Misra TK, Silver S (1990) Cloning, nucleotide sequence, and expression of the chromate resistance determinant of Pseudomonas aeruginosa plasmid pUM505. J Bacteriol 172:287–291

    PubMed  PubMed Central  CAS  Google Scholar 

  • Cervantes C, Campos-Garcia J, Gutierrez-Corona F, Loza-Tavera H, Torres-Guzman JC, Moreno-Sanchez R (2001) Interactions of chromium with microorganisms and plants. FEMS Microbiol Rev 25:335–347

    PubMed  CAS  Google Scholar 

  • Chang X, Li M, Liu Q, Liu Q, Yao J (2016) Adsorption-reduction of chromium (VI) from aqueous solution by phenol-formaldehyde resin microspheres. RSC Adv 6:46879

    CAS  Google Scholar 

  • Chen G, Fan J, Liu R, Zeng G, Chen A, Zou Z (2012) Removal of Cd (II), Cu (II) and Zn (II) from aqueous solutions by live Phanerochaete chrysosporium. Environ Technol 33(23):2653–2659

    PubMed  CAS  Google Scholar 

  • Chen Z, Song S, Wen Y (2016) Reduction of Cr (VI) into Cr (III) by organelles of Chlorella vulgaris in aqueous solution: an organelle-level attempt. Sci Total Environ 572:361–368

    PubMed  CAS  Google Scholar 

  • Cheung KH, Gu JD (2003) Reduction of chromate (CrO42−) by an enrichment consortium and an isolate of marine sulfate-reducing bacteria. Chemosphere 52:1523–1529

    PubMed  CAS  Google Scholar 

  • Cheung KH, Gu JD (2007) Mechanism of hexavalent chromium detoxification by microorganisms and bioremediation application potential: a review. Int Biodeterior Biodegrad 59:8–15

    CAS  Google Scholar 

  • Cheung KH, Lai HY, Gu JD (2006) Membrane-associated hexavalent chromium reductase of Bacillus megaterium TKW3 with induced expression. J Microbiol Biotechnol 16:855–862

    CAS  Google Scholar 

  • Chirwa EMN, Molokwane PE (2011) Biological Cr(VI) reduction: microbial diversity, kinetics and biotechnological solutions to pollution. In: Sofo A (ed) Biodiversity. InTech, Cambridge ISBN: 978-953-307-715-4

    Google Scholar 

  • Chrysochoou M, Johnston C (2012) Reduction of chromium (VI) in saturated zone sediments by calcium polysulfide and nanoscale zerovalent iron derived from green tea extract. Geotechnical Special Publication, 3959–3967. doi:https://doi.org/10.1061/9780784412121.406

  • Coeurdassier M, Devaufleury A, Scheifler R, Morhain E, Badot PM (2004) Effects of cadmium on the survival of three life-stages of the freshwater pulmonate Lymnaeastagnalis (Mollusca: Gastropoda). Bull Environ Contam Toxicol 72:1083–1090

    PubMed  CAS  Google Scholar 

  • Coleman RN (1988) Chromium toxicity: effects on microorganisms with special reference to the soil matrix. In: Nriagu JO, Nierboor E (eds) Chromium in the natural and human environments. Wiley, New York, pp 335–368

    Google Scholar 

  • Corradi MG, Gorbi G (1993) Chromium toxicity on two linked trophic levels. II Morphophysiological effects on Scenedesmus acutus. Ecotoxicol Environ Saf 25:72–78

    PubMed  CAS  Google Scholar 

  • Costa M (2003) Potential hazards of hexavalent chromate in our drinking water. Toxicol Appl Pharmacol 188:1–5

    PubMed  CAS  Google Scholar 

  • Czako-Ver K, Batie M, Raspor P, Sipiczki M, Pesti M (1999) Hexavalent chromium uptake by sensitive and tolerant mutants of Schizosaccharomyces pombe. FEMS Microbiol Lett 178:109–115

    PubMed  CAS  Google Scholar 

  • Das A, Chandra AL (1990) Chromate reduction in Streptomyces. Experientia 46:731e733

    Google Scholar 

  • Das S, Mishra J, Das S, Pandey S, Rao DS, Chakraborty A, Sudarshan M, Das N, Thatoi H (2014) Investigation on mechanism of Cr (VI) reduction and removal by Bacillus amyloliquefaciens, a novel chromate tolerant bacterium isolated from chromite mine soil. Chemosphere 96:112–121

    PubMed  CAS  Google Scholar 

  • Dayan AD, Paine AJ (2001) Mechanisms of chromium toxicity, carcinogenicity and allergenicity: review of the literature from 1985 to 2000. Human Expl Toxicol 20:439–451

    CAS  Google Scholar 

  • De Filippis LF, Pallaghy CK (1994) Heavy metals: sources and biological elects. In: Rai LC, Gaur JP, Soeder CJ (eds) Advances in limnology series: algae and water pollution. E. Scheizerbartsche Press, Stuttgart, pp 31–77

    Google Scholar 

  • Deng L, Wang H, Deng N (2006) Photoreduction of chromium (VI) in the presence of algae, Chlorella vulgaris. J Hazard Mater 138(2):288–292

    PubMed  CAS  Google Scholar 

  • Deng L, Zhang Y, Qin J, Wang X, Zhu X (2009) Biosorption of Cr (VI) from aqueous solutions by nonliving green algae Cladophora albida. Miner Eng 22:372–377

    CAS  Google Scholar 

  • Dey S, Paul AK (2012) Optimization of cultural conditions for growth associated chromate reduction by Arthrobacter sp. SUK 1201 isolated from chromite mine overburden. J Hazard Mater 213:200–206

    PubMed  Google Scholar 

  • Dhal B, Thatoi HN, Das NN, Pandeya BD (2013) Chemical and microbial remediation of hexavalent chromium from contaminated soil and mining/metallurgical solid waste: a review. J Hazard Mater 250:272–291

    PubMed  Google Scholar 

  • Dixit R, Malaviya D, Pandiyan K, Singh UB, Sahu A, Shukla R, Singh BP, Rai JP, Sharma PK, Lade H, Paul D (2015) Bioremediation of heavy metals from soil and aquatic environment: an overview of principles and criteria of fundamental processes. Sustainability 7(2):2189–2212

    CAS  Google Scholar 

  • Dvorak DH, Hedin RS, Edeborn HM, McIntire PE (1992) Treatment of metal-contaminated water using bacterial sulfate reduction: results from pilot-scale reactors. Biotechnol Bioeng 40:609–616

  • Efstathiou JD, McKay LL (1977) Inorganic salts resistance associated with a lactose-fermenting plasmid in Streptococcus lactis. J Bacteriol 13:257–265

    Google Scholar 

  • Elahi A, Rehman A (2017) Oxidative stress, chromium-resistance and uptake by fungi: isolated from industrial wastewater. Braz Arch Biol Technol 60:1–14

    Google Scholar 

  • Elahi A, Rehman A (2019a) Multiple metal resistance and Cr6+ reduction by bacterium, Staphylococcus sciuri A-HS1, isolated from untreated tannery effluent. J King Saud Uni Sci 31:1005–1013.0

    Google Scholar 

  • Elahi A, Rehman A (2019b) Comparative behavior of two gram positive Cr6+ resistant bacterial strains Bacillus aerius S1 and Brevibacterium iodinum S2 under hexavalent chromium stress. Biotechnol Rep 21:e00307

    Google Scholar 

  • Elahi A, Ajaz M, Rehman A, Vuilleumier S, Khan Z, Hussain SZ (2019) Isolation, characterization, and multiple heavy metal-resistant and hexavalent chromium-reducing Microbacterium testaceum B-HS2 from tannery effluent. J King Saud Uni Sci 31:1437–1444

    Google Scholar 

  • El-Sikaily A, El Nemr A, Khaled A, Abdelwehab O (2007) Removal of toxic chromium from wastewater using green alga Ulva lactuca and its activated carbon. J Hazard Mater 148:216–228

    PubMed  CAS  Google Scholar 

  • Environmental Protection Agency (EPA), 1998. Toxicological review for hexavalent chromium. CASNR. Washington DC, USA, 18540-29-9

  • Farag S, Zaki S (2010) Identification of bacterial strains from tannery effluent and reduction of hexavalent chromium. J Environ Biol 31(5):877

    CAS  Google Scholar 

  • Fasulo MP, Bassi M, Donini A (1983) Cytotoxic effects of hexavalent chromium in Euglena gracilis. II Physiological and ultrastructural studies. Protoplasma 114:35–43

    CAS  Google Scholar 

  • Francis AJ, Dodge CJ (1990) Anaerobic microbial remobilization of toxic metals coprecipitated with iron oxide. Environ Sci Technol 24:373–378

    CAS  Google Scholar 

  • Gheju M (2011) Hexavalent chromium reduction with zero-valent iron (ZVI) in aquatic systems. Water Air Soil Poll 222:103–148

    CAS  Google Scholar 

  • Gill TS, Pant JC (1987) Hematological and pathological effects of chromium toxicosis in the freshwater fish, Barbusconchonius ham. Water Air Soil Poll 35:241–250

    CAS  Google Scholar 

  • Gracia J, Green BF, Lundquist T, Mujeriego R, Hernandez-Marine M, Oswald WJ (2006) Long term diurnal variations on contaminant removal in high rate ponds treating urban wastewater. Bioresour Technol 97(14):1709–1715

    Google Scholar 

  • Graham AM, Bouwer EJ (2010) Rates of hexavalent chromium reduction in anoxic estuarine sediments: pH effects and the role of acid volatile sulfides. Environ Sci Technol 44:136–142

    PubMed  CAS  Google Scholar 

  • Gupta VK, Shrivastava AK, Jain N (2001) Biosorption of chromium (VI) from aqueous solutions by green algae Spirogyra sp. Water Res 35:4079–4085

    PubMed  CAS  Google Scholar 

  • Guria MK, Guha AK, Bhattacharyya M (2014) A green chemical approach for biotransformation of Cr (VI) to Cr (III), utilizing Fusarium sp. MMT1 and consequent structural alteration of cell morphology. J Environ Chem Eng 2(1):424–433

    CAS  Google Scholar 

  • Guttmann D, Poage G, Johnston T, Zhitkovich A (2008) Reduction with glutathione is a weakly mutagenic pathway in chromium (VI) metabolism. Chem Res Toxicol 21(11):2188–2194

    PubMed  PubMed Central  CAS  Google Scholar 

  • Halliwell B, Gutteridge JMC (1999) Free radicals in biology and medicine, 3rd edn. Oxford University Press, Oxford, pp 617–783

    Google Scholar 

  • He X, Hou B, Li C, Zhu Q, Jiang Y, Wu L (2014) Electrochemical mechanism of trivalent chromium reduction in 1-butyl-3-methylimidazolium bromide ionic liquid. Electrochim Acta 130:245

    CAS  Google Scholar 

  • Headlam HA, Lay PA (2016) Spectroscopic characterization of genotoxic chromium (V) peptide complexes: oxidation of chromium (III) triglycine, tetraglycine and pentaglycine complexes. J Inorg Biochem 162:227–237

    PubMed  CAS  Google Scholar 

  • Henson MW, Santo DJW, Kourtev PS, Jensen RV, Dunn JA, Learman DR (2015) Metabolic and genomic analysis elucidates strain-level variation in Microbacterium spp. isolated from chromate contaminated sediment. Peer J 3:e1395

    PubMed  Google Scholar 

  • Hussein KA, Joo JH (2013) Heavy metal resistance of bacteria and its impact on the production of antioxidant enzymes. African J Microbiol Res 7(20):2288–2296

    Google Scholar 

  • Hwang I, Batchelor B, Schlautman MA, Wang R (2002) Effects of ferrous iron and molecular oxygen on chromium (VI) redox kinetics in the presence of aquifer solids. J Hazard Mater 92(2):143–159

    PubMed  CAS  Google Scholar 

  • Igwe JC, Abia AA (2006) A bioseparation process for removing heavy metals from waste water using biosorbents. Afr J Biotechnol 5:1167–1179

    CAS  Google Scholar 

  • Jacobs J, Hardison RL, Rouse JV (2001) In-situ remediation of heavy metals using sulfur-based treatment technologies. Hydrovisions 10:1–4

    Google Scholar 

  • James BR (2002) Chemical transformations of chromium in soils—relevance to mobility, bio-availability and remediation: chromium file from the International Chromium Development Association, no. 8, February, 8

  • Joutey NT, Sayel H, Bahafid W, El Ghachtouli N (2015) Mechanisms of hexavalent chromium resistance and removal by microorganisms. Rev Environ Contam Toxicol 233:45–69

    PubMed  CAS  Google Scholar 

  • Jyoti J, Awasthi M (2014) Bioremediation of wastewater chromium through microalgae: a review. Int J Eng Res Technol 3:1210–1215

    Google Scholar 

  • Kang SY, Lee JU, Moon SH, Kim KW (2004) Competitive adsorption characteristics of Co+2, Ni+2 and Cr+3 by IRN-77 cation exchange resin in synthesized wastewater. J Chem 56:141–147

    CAS  Google Scholar 

  • Kouadjo CG, Zeze A (2011) Chromium tolerance and reduction potential of staphylococci species isolated from a fly ash dumping site in South Africa. Afr J Biotechnol 10(69):5587–5594

    Google Scholar 

  • Kourtev PS, Nakatsu CH, Konopka A (2009) Inhibition of nitrate reduction by chromium (VI) in aerobic soil microsomes. Appl Environ Microbiol 75:3249–6257

    Google Scholar 

  • Krieg NR, Hoffman PS (1986) Microaerophily and oxygen toxicity. Ann Rev Microbiol 40:107–130

    CAS  Google Scholar 

  • Ksheminska H, Fedorovych D, Babyak L, Yanovych D, Kaszycki P, Koloczek H (2005) Chromium (III) and (VI) tolerance and bioaccumulation in yeast: a survey of cellular chromium content in selected strains of representative genera. Process Biochem 40(5):1565–1572

    CAS  Google Scholar 

  • Lalith Varadhan S, Mohan S (2017) Selection and use of efficient bacterial strains for chromium biosorption in tannery effluent. Int J Recent Sci Res 8:16230–16233

    Google Scholar 

  • Lee L, Hsu CY, Yen HW (2017) The effects of hydraulic retention time (HRT) on chromium (VI) reduction using autotrophic cultivation of Chlorella vulgaris. Bioprocess Biosyst Eng 40(12):1725–1731

    PubMed  CAS  Google Scholar 

  • Losi ME, Amrhein C, Frankenberger WT (1994) Environmental biochemistry of chromium. Rev Environ Contam Toxicol 36:91–121

    Google Scholar 

  • Mala JGS, Nair BU, Puvanakrishnan R (2006) Bioaccumulation and biosorption of chromium by Aspergillus niger MTCC 2594. J Gen Appl Microbiol 52(3):179–186

    CAS  Google Scholar 

  • Malaviya P, Singh A (2016) Bioremediation of chromium solutions and chromium containing wastewaters. Crit Rev Microbiol 42(4):607–633

    PubMed  CAS  Google Scholar 

  • Mani D, Kumar C (2013) Biotechnological advances in bioremediation of heavy metals contaminated ecosystems: an overview with special reference to phytoremediation. Int J Environ Sci Technol 11(3):843–872

    Google Scholar 

  • McGrath SP, Smith S (1990) Chromium and nickel. In: Alloway BJ (ed) Heavy metals in soils. Wiley, New York, pp 125–150

    Google Scholar 

  • Meegoda JN, Kamolpornwijit W, Batagoda JH (2017) A detailed laboratory scale feasibility study of recovering metallic iron and chromium from chromium contaminated soils. Indian Geotech J 47(4):437–444

    Google Scholar 

  • Messer J, Reynolds M, Stoddard L, Zhitkovich A (2006) Causes of DNA single-strand breaks during reduction of chromate by glutathione in vitro and in cells. Free Radic Biol Med 40:1981–1992

    PubMed  CAS  Google Scholar 

  • Min M, Wang L, Li Y, Mohr MJ, Hu B, Zhou W, Chen P, Ruan R (2011) Cultivating Chlorella sp. in a pilot-scale photobioreactor using centrate wastewater for microalgae biomass production and wastewater nutrient removal. Appl Biochem Biotechnol 165:123–137

    PubMed  CAS  Google Scholar 

  • Miransari M (2011) Hyperaccumulators, arbuscular mycorrhizal fungi and stress of heavy metals. Biotechnol Adv 29(6):645–653

    PubMed  CAS  Google Scholar 

  • Mistry K, Desai C, Lal S, Patel K, Patel B (2010) Hexavalent chromium reduction by Staphylococcus sp. isolated from Cr (VI) contaminated land fill. Int J Biotechnol Biochem 6(1):117–129

    Google Scholar 

  • Mona S, Kaushik A, Kaushik CP (2011) Biosorption of chromium (VI) by spent cyanobacterial biomass from a hydrogen fermenter using Box-Behnken model. Int Biodeterior Biodegrad 65:656–663

    CAS  Google Scholar 

  • Mondaca MA, Gonzalez CL, Zaror CA (1998) Isolation, characterization and expression of a plasmid encoding chromate resistance in Pseudomonas putida KT2441. Appl Microbiol Lett 26:367–371

    CAS  Google Scholar 

  • Morales-Barrera L, Guillén-Jimenéz FM, Ortiz-Moreno A, Villegas-Garrido TL, Sandoval-Cabrera A, Hernéndez-Rodríguez CH, Cristiani-Urbina E (2008) Isolation, identification and characterization of a Hypocrea tawa, strain with high Cr(VI) reduction potential. Biochem Eng J 40:284–292

    CAS  Google Scholar 

  • Narayani M, Vidya KS (2012) Characteristics of a novel Acinetobacter sp. and its kinetics in hexavalent chromium bioreduction. J Microbiol Biotechnol 22(5):690–698

    PubMed  CAS  Google Scholar 

  • Nies A, Nies DH, Silver S (1989) Cloning and expression of plasmid genes encoding resistance to chromate and cobalt in Alcaligenes eutrophus. J Bacteriol 171:5065–5070

    PubMed  PubMed Central  CAS  Google Scholar 

  • Nies A, Nies DH, Silver S (1990) Nucleotide sequence and expression of a plasmid-encoded chromate resistance determinant from Alcaligenes eutrophus. J Biol Chem 265:5648–5653

    PubMed  CAS  Google Scholar 

  • Ohtake H, Silver S (1994) Bacterial detoxification of toxic chromate. In: Chaudhry GR (ed) Biological degradation and bioremediation of toxic chemicals. Dioscorides, Portland, pp 403–415

    Google Scholar 

  • Ohtake H, Cervantes C, Silver S (1987) Decreased chromate uptake in Pseudomonas fluorescens carrying a chromate resistance plasmid. J Bacteriol 169:3853–3856

    PubMed  PubMed Central  CAS  Google Scholar 

  • Papp JF (1985) Chromium. In: Knoerr AW (ed) Mineral facts and problems: Bureau of Mines Bulletin 675. US Government Printing Office, Washington, pp 139–155

    Google Scholar 

  • Park CH, Gonzalez D, Ackerley D, Keyhan M, Matin A (2002) Molecular engineering of soluble bacterial proteins with chromate reductase activity. In: Pellei M, Porta A, Hinchee RE (eds) Remediation and beneficial reuse of contaminated sediments, vol 3. Batelle Press, Columbus, pp 103–112

    Google Scholar 

  • Pattanapipitpaisal P, Brown NL, Macaskie LE (2001) Chromate reduction and 16S rRNA identification of bacteria isolated from a Cr (VI)-contaminated site. Appl Microbiol Biotechnol 57:257–261

    PubMed  CAS  Google Scholar 

  • Peitzsch N, Eberz G, Nies DH (1998) Alcaligenes eutrophus as a bacterial chromate sensor. Appl Environ Microbiol 64:453–458

    PubMed  PubMed Central  CAS  Google Scholar 

  • Pillichshammer M, Pumpel T, Poder R, Eller K, Klima J, Schinner F (1995) Biosorption of chromium to fungi. BioMetals 8:117–121

    CAS  Google Scholar 

  • Pradhan D, Kim DJ, Ahn JG, Chaudhury GR, Lee SW (2010) Kinetics and statistical behavior of metals dissolution from spent petroleum catalyst using acidophilic iron oxidizing bacteria. J Ind Eng Chem 16(5):866–871

    CAS  Google Scholar 

  • Pradhan D, Sukla L, Sawyer M, Rahman P (2017) Recent bioreduction of hexavalent chromium in wastewater treatment: a review. J Indus Eng Chem 55:1–20

    CAS  Google Scholar 

  • Puzon GJ, Petersen JN, Roberts AG, Kramer DM, Xun L (2002) A bacterial flavin reductase system reduces chromate to soluble chromium (III)-NAD+ complex. Biochem Biophys Res Commun 294:76–81

    PubMed  CAS  Google Scholar 

  • Qamar M, Gondal MA, Yamani ZH (2011) Synthesis of nanostructured NiO and its application in laser-induced photocatalytic reduction of Cr (VI) from water. J Mol Catal A Chem 341(1):83–88

    CAS  Google Scholar 

  • Ramanathan S, Ensor M, Daunert S (1997) Bacterial biosensors for monitoring toxic metals. Trends Biotechnol 15:501–506

    Google Scholar 

  • Ramirez-Ramirez R, Calvo-Mendez C, Avila-Rodriguez M, Lappe P, Ulloa M, Vazquez-Suarez R, Gutierrez-Corona F (2004) Cr(VI) reduction in a chromate resistant strain of Candida maltosa isolated from the leather industry. Anton Leeuw 85:63–68

    CAS  Google Scholar 

  • Rehman A, Anjum MS (2011) Multiple metal tolerance and biosorption of cadmium by Candida tropicalis isolated from industrial effluents: glutathione as detoxifying agent. Environ Monit Assess 174:585–595

    PubMed  CAS  Google Scholar 

  • Rehman A, Shakoori AR (2001) Heavy metal resistant Chlorella spp., isolated from tannery effluents, and their role in remediation of hexavalent chromium in industrial wastewater. Bull Environ Contam Toxicol 66(2):542–547

    PubMed  CAS  Google Scholar 

  • Rezaei H (2013) Biosorption of chromium by using Spirulina sp. Arab J Chem 9:846–853

    Google Scholar 

  • Romanenko VI, Korenkov VN (1977) A pure culture of bacterial cells assimilating chromates and bichromates as hydrogen acceptors when grown under anaerobic conditions. Mikrobiologiya 46:414–417

    CAS  Google Scholar 

  • Ryan DR, Leukes WD, Burton SG (2005) Fungal bioremediation of phenolic wastewaters in an airlift reactor. Biotechnol Prog 21(4):1068–1074

    PubMed  CAS  Google Scholar 

  • Sagar S, Dwivedi A, Yadav S, Tripathi M, Kaistha SD (2012) Hexavalent chromium reduction and plant growth promotion by Staphylococcus arlettae strain Cr11. Chemosphere 86:847–852

    PubMed  CAS  Google Scholar 

  • Sari A, Tuzen M (2008) Biosorption of total chromium from aqueous solution by red algae (Ceramium virgatum): equilibrium, kinetic and thermodynamic studies. J Hazard Mater 160:349–355

    PubMed  CAS  Google Scholar 

  • Sawyer CN, McCarty PL, Parkin GF (1994) Chemistry for environmental engineering, 4th edn. McGraw-Hill, New York

    Google Scholar 

  • Sen M, Dastidar MG (2010) Chromium removal using various biosorbents. Iran J Environ Health Sci Eng 7:182–190

    Google Scholar 

  • Shanab S, Essa A, Shalaby E (2012) Bioremoval capacity of three heavy metals by some micro algae species (Egyptian isolates). Plant Signal Behav 7:1–8

    Google Scholar 

  • Shewry PR, Peterson PJ (1976) Distribution of chromium and nickel in plants and soil from serpentine and other sites. J Ecol 64:195–212

    CAS  Google Scholar 

  • Singh J, Carlisle DL, Pritchard DE, Patierno SR (1998) Chromium-induced genotoxicity and apoptosis: relationship to chromium carcinogenesis (review). Oncol Rep 5:1307–1318

    PubMed  CAS  Google Scholar 

  • Somasundaram V, Philip L, Bhallamudi SM (2011) Laboratory scale column studies on transport and biotransformation of Cr (VI) through porous media in presence of CRB, SRB and IRB. Chem Eng J 171(2):572–581

    CAS  Google Scholar 

  • Srivastava S, Thakur IS (2006) Isolation and process parameter optimization of Aspergillus sp. for removal of chromium from tannery effluent. Bioresour Technol 97:1167–1173

    PubMed  CAS  Google Scholar 

  • Stern RM (1982) Chromium compounds: production and occupational exposure. In: Langard S (ed) Biological and environmental aspects of chromium. Elsevier, Amsterdam, pp 5–47

    Google Scholar 

  • Sudhakar G, Jyothi B, Venkateswarlu V (1991) Metal pollution and its impact on algae in flowing waters in India. Arch Environ Contam Toxicol 21:556–566

    PubMed  CAS  Google Scholar 

  • Sultan S, Hasnain S (2007) Reduction of toxic hexavalent chromium by Ochrobactrum intermedium strain SDCr-5 stimulated by heavy metals. Bioresour Technol 98:340–344

    PubMed  CAS  Google Scholar 

  • Suzuki Y, Fukuda K (1990) Reduction of hexavalent chromium by ascorbic acid and glutathione with special reference to the rat lung. Arch Toxicol 64(3):169–176

    PubMed  CAS  Google Scholar 

  • Tam NFY, Wong YS (1989) Wastewater nutrient removal by Chlorella pyrenoidosa and Scenedesmus sp. Environ Pollut 58:19–34

    PubMed  CAS  Google Scholar 

  • Thatoi H, Das S, Mishra J, Rath BP, Das N (2014) Bacterial chromate reductase, a potential enzyme for bioremediation of hexavalent chromium: a review. J Environ Manag 146:383–399

    CAS  Google Scholar 

  • Thiele DJ (1995) Metal detoxification in eukaryotic cells. Crisp Data Base of National Institute of Health, Washington

    Google Scholar 

  • Turnau K, Orlowska E, Ryszka P, Zubek S, Anielska T, Gawronski S, Jurkiewicz A (2006) Role of mycorrhizal fungi in phytoremediation and toxicity monitoring of heavy metal rich industrial wastes in southern Poland. In: Twardowska I, Allen HE, Häggblom MM, Stefaniak S (eds) Soil and water pollution monitoring, protection and remediation. NATO science series, vol 69. Springer, Dordrecht

    Google Scholar 

  • Turner MA, Rust RH (1971) Effects of chromium on growth and mineral nutrition of soybeans. Soil Sci Soc Am J 35:755–758

    CAS  Google Scholar 

  • Unz RF, Shuttleworth KL (1996) Microbial mobilization and immobilization of heavy metals. Curr Opin Biotechnol 7:307–310

    PubMed  CAS  Google Scholar 

  • U.S. Geological Survey (2016) National Water Information System data available on the World Wide Web (USGS Water Data for the Nation). https://waterdata.usgs.gov/nwis/. Accessed 10 Jun 2017

  • Vankar PS, Bajpai D (2007) Phytoremediation of chromium VI of tannery effluent by Trichoderma sp. In: Conference on desalination and the environment. Sponsored by the European Desalination Society and Center for Research and Technology Hellas (CERTH), Sani resort, Halkidiki, Greece. April 22–25

  • Viamajala S, Peyton BM, Sani RK, Apel WA, Petersen JN (2004) Toxic effects of chromium (VI) on anaerobic and aerobic growth of Shewanella oneidensis MR-1. Biotechnol Prog 20:87–95

    PubMed  CAS  Google Scholar 

  • Vincent JB (2017) New evidence against chromium as an essential trace element. J Nutr 147(12):2212–2219

    PubMed  CAS  Google Scholar 

  • Volesky B, Holan ZR (1995) Biosorption of heavy metals. Biotechnol Prog 11:235–250

    PubMed  CAS  Google Scholar 

  • Vymazal J (1990) Uptake of lead, chromium, cadmium and cobalt by Cladophora glomerata. Bull Environ Contam Toxicol 44:468–472

    PubMed  CAS  Google Scholar 

  • Wakatsuki T (1995) Metal oxidoreduction by microbial cells. J Ind Microbiol 14:169–177

    PubMed  CAS  Google Scholar 

  • Wales DS, Sagar BF (1990) Recovery of metal ions by microfungal filters. J Chem Technol Biotechnol 49:345–355

    PubMed  CAS  Google Scholar 

  • Wallwork GR (1976) The oxidation of alloys. Rep Prog Phys 39:401

    CAS  Google Scholar 

  • Wang L, Wang N, Zhu L, Yu H, Tang H (2008) Photocatalytic reduction of Cr (VI) over different TiO2 photocatalysts and the effects of dissolved organic species. J Hazard Mater 152:93–99

    PubMed  CAS  Google Scholar 

  • Wang L, Min M, Li Y, Chen P, Chen Y, Liu Y, Wang Y, Ruan R (2010) Cultivation of green algae Chlorella sp. in different wastewaters from municipal wastewater treatment plant. Appl Biochem Biotechnol 162:1174–1186

    PubMed  CAS  Google Scholar 

  • Wani R, Kodam KM, Gawai KR, Dhakephalkar PK (2007) Chromate reduction by Burkholderia cepacia MCMB-821, isolated from the pristine habitat of alkaline Crater Lake. Appl Microbiol Biotechnol 75:627–632

    PubMed  CAS  Google Scholar 

  • Westbrook J (1983) Chromium and chromium alloys. In: Grayson M (ed) Kirk-Othmer encyclopedia of chemical technology, vol 54, 3rd edn. Wiley-Interscience, New York

    Google Scholar 

  • Wu G, Kang H, Zhang X, Shao H, Chu L, Ruan C (2010) A critical review on the bio-removal of hazardous heavy metals from contaminated soils: issues, progress, eco-environmental concerns and opportunities. J Hazard Mater 174:1–8

    PubMed  CAS  Google Scholar 

  • Yadav M, Xu Q (2013) Catalytic chromium reduction using formic acid and metal nanoparticles immobilized in a metal–organic framework. Chem Commun 49:3327

    CAS  Google Scholar 

  • Ye J, Yin H, Mai B, Peng H, Qin H, He B, Zhang N (2010) Biosorption of chromium from aqueous solution and electroplating wastewater using mixture of Candida lipolytica and dewatered sewage sludge. Bioresour Technol 101(11):3893–3902

    PubMed  CAS  Google Scholar 

  • Yuan Y, Yang S, Zhou D, Wu F (2016) A simple Cr(VI)-S(IV)-O2 system for rapid and simultaneous reduction of Cr(VI) and oxidative degradation of organic pollutants. J Hazard Mater 307:294–301

    PubMed  CAS  Google Scholar 

  • Zahoor A, Rehman A (2009) Isolation of Cr (VI) reducing bacteria from industrial effluents and their potential use in bioremediation of chromium containing wastewater. J Environ Sci 21:814–820

    Google Scholar 

  • Zhang K, Li F (2011) Isolation and characterization of a chromium-resistant bacterium Serratia sp. Cr-10 from a chromate-contaminated site. Appl Microbiol Biotechnol 90(3):1163–1169

    PubMed  CAS  Google Scholar 

  • Zhitkovich A (2005) Importance of chromium-DNA adducts in mutagenicity and toxicity of chromium (VI). Chem Res Toxicol 18:3–11

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology and Molecular Genetics, University of the Punjab, New Campus, Lahore, 54590, Pakistan

    Amina Elahi & Abdul Rehman

  2. Department of Microbiology and Molecular Genetics, The Women University, Multan, Pakistan

    Iqra Arooj

  3. Department of Zoology, Government College University, Lahore, Pakistan

    Dilara A. Bukhari

Authors
  1. Amina Elahi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Iqra Arooj
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dilara A. Bukhari
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Abdul Rehman
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

AE designed the study and wrote the article. IA and DAB helped in data collection and in manuscript editing. AR contributed in the design, write-up, and final editing of the manuscript. All authors read and approved the manuscript.

Corresponding author

Correspondence to Abdul Rehman.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethical statement

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(PDF 638 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Elahi, A., Arooj, I., Bukhari, D.A. et al. Successive use of microorganisms to remove chromium from wastewater. Appl Microbiol Biotechnol 104, 3729–3743 (2020). https://doi.org/10.1007/s00253-020-10533-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-020-10533-y

Keywords

Search

Navigation