Skip to main content
Log in

Microbial interactions with chromium: basic biological processes and applications in environmental biotechnology

  • REVIEW
  • Published:
World Journal of Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Chromium (Cr) is a highly toxic metal for microorganisms as well as plants and animal cells. Due to its widespread industrial use, Cr has become a serious pollutant in diverse environmental settings. The hexavalent form of the metal, Cr(VI), is considered a more toxic species than the relatively innocuous and less mobile Cr(III) form. The study of the interactions between microorganisms and Cr has been helpful to unravel the mechanisms allowing organisms to survive in the presence of high concentrations of Cr(VI) and to detoxify and remove the oxyanion. Various mechanisms of interactions with Cr have been identified in diverse species of bacteria and fungi, including biosorption, bioaccumulation, reduction of Cr(VI) to Cr(III), and chromate efflux. Some of these systems have been proposed as potential biotechnological tools for the bioremediation of Cr pollution using bioreactors or by in situ treatments. In this review, the interactions of microorganisms with Cr are summarised, emphasising the importance of new research avenues using advanced methodologies, including proteomic, transcriptomic, and metabolomic analyses, as well as the use of techniques based on X-ray absorption spectroscopy and electron paramagnetic resonance spectroscopy.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abigail EA, Samuel MS, Chidambaram R (2015) Hexavalent chromium biosorption studies using Penicillium griseofulvum MSR1 a novel isolate from tannery effluent site: Box–Behnken optimization, equilibrium, kinetics and thermodynamic studies. J Taiwan Inst Chem E 49:156–164

    Article  Google Scholar 

  • Ahmad WA, Zakaria ZA, Khasim AR et al (2010) Pilot-scale removal of chromium from industrial wastewater using the ChromeBac™ system. Bioresour Technol 101:4371–4378

    Article  CAS  Google Scholar 

  • Annamalai K, Nair AM, Chinnaraju S, Kuppusamy S (2014) Removal of chromium from contaminated effluent and simultaneously green nanoparticle synthesis using Bacillus subtilis. Malaya J Biosci 1:13–18

    CAS  Google Scholar 

  • Arévalo-Rangel DL, Cárdenas-González JF, Martínez-Juárez VM, Acosta-Rodríguez I (2013) Hexavalent chromate reductase activity in cell free extracts of Penicillium sp. Bioinorg Chem Appl 2013:1–6

    Article  Google Scholar 

  • Bahafid W, Joutey NT, Sayel H et al (2013) Bioaugmentation of chromium-polluted soil microcosms with Candida tropicalis diminishes phytoavailable chromium. J Appl Microbiol 115:727–734

    Article  CAS  Google Scholar 

  • Balaji R, David E (2016) Isolation and characterization of Cr(VI) reducing bacteria and fungi their potential use in bioremediation of chromium containing tannery effluent (Ambur and Ranipet, Vellore dist, Tamilnadu). Adv Res J Life Sci 2:1–4

    Google Scholar 

  • Bankar AV, Kumar AR, Zinjarde SS (2009) Removal of chromium (VI) ions from aqueous solution by adsorption onto two marine isolates of Yarrowia lipolytica. J Hazard Mater 170:487–494

    Article  CAS  Google Scholar 

  • Barak Y, Ackerley DF, Dodge CJ et al (2006) Analysis of novel soluble chromate and uranyl reductases and generation of an improved enzyme by directed evolution. Appl Environ Microb 72:7074–7082

    Article  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 223:1–12

    Article  Google Scholar 

  • Barsainya M, Chandra P, Singh DP (2016) Investigation of Cr(VI) uptake in saline condition using psychrophilic and mesophilic Penicillium sp. Int J Curr Microbiol Appl Sci 5:274–288

    Article  Google Scholar 

  • Bencheikh-Latmani R, Obraztsova A, Mackey MR, Ellisman MH, Tebo BM (2007) Toxicity of Cr(III) to Shewanella sp. strain MR-4 during Cr(VI) reduction. Environ Sci Technol 41:214–220

    Article  CAS  Google Scholar 

  • Cervantes C, Campos-García J, Devars S et al (2001) Interactions of chromium with microorganisms and plants. FEMS Microbiol Rev 25:335–347

    Article  CAS  Google Scholar 

  • Chang F, Tian C, Liu S et al (2016) Discrepant hexavalent chromium tolerance and detoxification by two strains of Trichoderma asperellum with high homology. Chem Eng J 298:75–81

    Article  CAS  Google Scholar 

  • Chatterjee S, Ghosh I, Mukherjea KK (2011) Uptake and removal of toxic Cr(VI) by Pseudomonas aeruginosa: physico-chemical and biological evaluation. Curr Sci India 101:645–652

    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(1):8–15

    Article  CAS  Google Scholar 

  • Coreño-Alonso A, Solé A, Diestra E, Esteve I, Gutiérrez-Corona JF, Reyna López GE, Fernández FJ, Tomasini A (2014) Mechanisms of interaction of chromium with Aspergillus niger var tubingensis strain Ed8. Bioresour Technol 158:188–192

    Article  Google Scholar 

  • Dey S, Paul AK (2016) Evaluation of chromate reductase activity in the cell-free culture filtrate of Arthrobacter sp. SUK 1201 isolated from chromite mine overburden. Chemosphere 156:69–75

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Díaz-Pérez C, Cervantes C, Campos-García J et al (2007) Phylogenetic analysis of the chromate ion transporter (CHR) superfamily. FEBS J 274:6215–6227

    Article  Google Scholar 

  • Dogan NM, Doganli GA, Dogan G et al (2015) Characterization of extracellular polysaccharides (EPS) produced by thermal Bacillus and determination of environmental conditions affecting exopolysaccharide production. Int J Environ Res 9:1107–1116

    CAS  Google Scholar 

  • Dong G, Wang Y, Gong L et al (2013) Formation of soluble Cr(III) end-products and nanoparticles during Cr(VI) reduction by Bacillus cereus strain XMCr-6. Biochem Eng J 70:166–172

    Article  CAS  Google Scholar 

  • Flores-Alvarez L, Corrales-Escobosa A, Cortés-Penagos C et al (2012) The Neurospora crassa chr-1 gene is up-regulated by chromate and its encoded CHR-1 protein causes chromate sensitivity and chromium accumulation. Curr Genet 58:281–290

    Article  CAS  Google Scholar 

  • Gu Y, Xu W, Liu Y et al (2015) Mechanism of Cr(VI) reduction by Aspergillus niger: enzymatic characteristic, oxidative stress response, and reduction product. Environ Sci Pollut R 22:6271–6279

    Article  CAS  Google Scholar 

  • Habibul N, Hu Y, Wang YK et al (2016) Bioelectrochemical chromium (VI) removal in plant-microbial fuel cells. Environ Sci Technol 50:3882–3889

    Article  CAS  Google Scholar 

  • Holland SL, Avery SV (2009) Actin-mediated endocytosis limits intracellular Cr accumulation and Cr toxicity during chromate stress. Toxicol Sci 111:437–446

    Article  CAS  Google Scholar 

  • Ishak AF, Karim NA, Ahmad WA et al (2016) Chromate detoxification using combination of ChromeBac™ system and immobilized chromate reductase beads. Int Biodeterior Biodegrad 113:238–243

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Kathiravan MN, Rani RK, Karthick R et al (2010) Mass transfer studies on the reduction of Cr(VI) using calcium alginate immobilized Bacillus sp. in packed bed reactor. Bioresour Technol 101:853–858

    Article  CAS  Google Scholar 

  • Khambhaty Y, Mody K, Basha S, Jha B (2009) Kinetics, equilibrium and thermodynamic studies on biosorption of hexavalent chromium by dead fungal biomass of marine Aspergillus niger. Chem Eng J 145:489–495

    Article  CAS  Google Scholar 

  • Krishna KR, Philip L (2005) Bioremediation of Cr(VI) in contaminated soils. J Hazard Mater 121(1):109–117

    Article  CAS  Google Scholar 

  • Latha S, Vinothini G, Dhanasekaran D (2015) Chromium [Cr(VI)] biosorption property of the newly isolated actinobacterial probiont Streptomyces werraensis LD22. Biotech 5:423–432

    Google Scholar 

  • Liu H, Huang J, Zhang S et al (2015) Chromate interaction with the chromate reducing actinobacterium intrasporangium chromatireducens Q5-1. Geomicrobiol J 32:616–623

    Article  CAS  Google Scholar 

  • Madhavi V, Reddy AVB, Reddy KG et al (2013) An overview on research trends in remediation of chromium. Res J Recent Sci 2:71–83

    CAS  Google Scholar 

  • Marandi R (2011) Biosorption of hexavalent chromium from aqueous solution by dead fungal biomass of Phanerochaete crysosporium: batch and fixed bed studies. Can J Chem Eng Technol 2:8–22

    Google Scholar 

  • Mohan D, Pittman CU (2006) Activated carbons and low cost adsorbents for remediation of tri-and hexavalent chromium from water. J Hazard Mater 137(2):762–811

    Article  CAS  Google Scholar 

  • Mohite PT, Kumar AR, Zinjarde SS (2015) Biotransformation of hexavalent chromium into extracellular chromium (III) oxide nanoparticles using Schwanniomyces occidentalis. Biotechnol Lett 2015:1–6

    Google Scholar 

  • Morales-Barrera L, Cristiani-Urbina E (2006) Removal of hexavalent chromium by Trichoderma viride in an airlift bioreactor. Enzyme Microb Technol 40:107–113

    Article  CAS  Google Scholar 

  • Mukherjee K, Saha R, Ghosh A et al (2013) Chromium removal technologies. Res Chem Intermediat 39(6):2267–2286

    Article  CAS  Google Scholar 

  • Naik UC, Srivastava S, Thakur IS (2012) Isolation and characterization of Bacillus cereus IST105 from electroplating effluent for detoxification of hexavalent chromium. Environ Sci Pollut Res Int 19:3005–3014

    Article  CAS  Google Scholar 

  • Ozturk S, Aslim B (2008) Relationship between chromium(VI) resistance and extracellular polymeric substances (EPS) concentration by some cyanobacterial isolates. Environ Sci Pollut Res 15:478–480

    Article  CAS  Google Scholar 

  • Pang Y, Zeng GM, Tang L et al (2011) Cr(VI) reduction by Pseudomonas aeruginosa immobilized in a polyvinyl alcohol/sodium alginate matrix containing multi-walled carbon nanotubes. Bioresour Technol 102:10733–10736

    Article  CAS  Google Scholar 

  • Park D, Yun YS, Park JM (2005) Use of dead fungal biomass for the detoxification of hexavalent chromium: screening and kinetics. Process Biochem 40:2559–2565

    Article  CAS  Google Scholar 

  • Park D, Yun YS, Park JM (2006) Mechanisms of the removal of hexavalent chromium by biomaterials or biomaterial-based activated carbons. J Hazard Mater 137(2):1254–1257

    Article  CAS  Google Scholar 

  • Park D, Lim SR, Yun YS et al (2007) Reliable evidences that the removal mechanism of hexavalent chromium by natural biomaterials is adsorption-coupled reduction. Chemosphere 70:298–305

    Article  CAS  Google Scholar 

  • Paul ML, Samuel J, Chandrasekaran N et al (2012) Comparative kinetics, equilibrium, thermodynamic and mechanistic studies on biosorption of hexavalent chromium by live and heat killed biomass of Acinetobacter junii VITSUKMW2, an indigenous chromite mine isolate. Chem Eng J 187:104–113

    Article  CAS  Google Scholar 

  • Poljsak B, Pócsi I, Raspor P et al (2010) Interference of chromium with biological systems in yeasts and fungi: a review. J Basic Microb 50:21–36

    Article  CAS  Google Scholar 

  • Polti MA, Amoroso MJ, Abate CM (2011) Intracellular chromium accumulation by Streptomyces sp. MC1. Water Air Soil Pollut 214:49–57

    Article  CAS  Google Scholar 

  • Qian J, Wei L, Liu R et al (2016) An exploratory study on the pathways of Cr(VI) reduction in sulfate-reducing up-flow anaerobic sludge bed (UASB) reactor. Sci Rep 6:23694

    Article  CAS  Google Scholar 

  • Ramírez-Díaz M, Díaz-Pérez C, Vargas E et al (2008) Mechanisms of bacterial resistance to chromium compounds. Biometals 21:321–332

    Article  Google Scholar 

  • Ramrakhiani L, Majumder R, Khowala S (2011) Removal of hexavalent chromium by heat inactivated fungal biomass of Termitomyces clypeatus: surface characterization and mechanism of biosorption. Chem Eng J 171:1060–1068

    Article  CAS  Google Scholar 

  • Rath BP, Das S, Mohapatra PKD et al (2014) Optimization of extracellular chromate reductase production by Bacillus amyloliquefaciens (CSB 9) isolated from chromite mine environment. Biocatal Agric Biotechnol 3:35–41

    Google Scholar 

  • Robins KJ, Hooks DO, Rehm BH et al (2013) Escherichia coli NemA is an efficient chromate reductase that can be biologically immobilized to provide a cell free system for remediation of hexavalent chromium. PLoS One 8:e59200

    Article  CAS  Google Scholar 

  • Romo-Rodríguez P, Acevedo-Aguilar FJ, Lopez-Torres A et al (2015) Cr(VI) reduction by gluconolactone and hydrogen peroxide, the reaction products of fungal glucose oxidase: cooperative interaction with organic acids in the biotransformation of Cr(VI). Chemosphere 134:563–570

    Article  Google Scholar 

  • Samuel J, Pulimi M, Paul ML et al (2013) Batch and continuous flow studies of adsorptive removal of Cr(VI) by adapted bacterial consortia immobilized in alginate beads. Bioresour Technol 128:423–430

    Article  CAS  Google Scholar 

  • Samuel MS, Abigail MEA, Ramalingam C (2015) Isotherm modelling, kinetic study and optimization of batch parameters using response surface methodology for effective removal of Cr(VI) using fungal biomass. PLoS One 10:e0116884

    Article  Google Scholar 

  • Seo H, Roh Y (2015) Biotransformation and its application: biogenic nano-catalyst and metal-reducing-bacteria for remediation of Cr(VI)-contaminated water. J Nanosci Nanotechnol 15:5649–5652

    Article  CAS  Google Scholar 

  • Sepehr MN, Nasseri S, Zarrabi M et al (2012a) Removal of Cr(III) from tanning effluent by Aspergillus niger in airlift bioreactor. Sep Purif Technol 96:256–262

    Article  CAS  Google Scholar 

  • Sepehr MN, Zarrabi M, Amrane A (2012b) Removal of CR (III) from model solutions by isolated Aspergillus niger and Aspergillus oryzae living microorganisms: equilibrium and kinetic studies. J Taiwan Inst Chem E 43:420–427

    Article  CAS  Google Scholar 

  • Sharma S, Malaviya P (2016) Bioremediation of tannery wastewater by chromium resistant novel fungal consortium. Ecol Eng 91:419–425

    Article  Google Scholar 

  • Shroff KA, Vaidya VK (2012) Effect of pre-treatments on the biosorption of Chromium (VI) ions by the dead biomass of Rhizopus arrhizus. J Chem Technol Biotechnol 87:294–304

    Article  CAS  Google Scholar 

  • Shuhong Y, Meiping Z, Hong Y et al (2014) Biosorption of Cu(2+), Pb(2+) and Cr(6+) by a novel exopolysaccharide from Arthrobacter ps-5. Carbohydr Polym 101:50–56

    Article  Google Scholar 

  • Silva B, Figueiredo H, Quintelas C et al (2012) Improved biosorption for Cr(VI) reduction and removal by Arthrobacter viscosus using zeolite. Int Biodeterior Biodegrad 74:116–123

    Article  CAS  Google Scholar 

  • Singh R, Bishnoi NR (2015) Biotransformation dynamics of chromium (VI) detoxification using Aspergillus flavus system. Ecol Eng 75:103–109

    Article  Google Scholar 

  • Somasundaram V, Philip L, Bhallamudi SM (2009) Experimental and mathematical modeling studies on Cr(VI) reduction by CRB, SRB and IRB, individually and in combination. J Hazard Mater 172:606–617

    Article  CAS  Google Scholar 

  • Sukumar C, Janaki V, Kamala-Kannan K, Shanthi K (2014) Biosorption of chromium(VI) using Bacillus subtilis SS-1 isolated from soil samples of electroplating industry. Clean Technol Environ Policy 16:405–413

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Tripathi M, Garg SK (2013) Co-remediation of pentachlorophenol and Cr6+ by free and immobilized cells of native Bacillus cereus isolate: spectrometric characterization of PCP dechlorination products, bioreactor trial and chromate reductase activity. Process Biochem 48:496–509

    Article  CAS  Google Scholar 

  • Viti C, Marchi E, Decorosi F, Giovannetti L (2014) Molecular mechanisms of Cr(VI) resistance in bacteria and fungi. FEMS Microbiol Rev 38:633–659

    Article  CAS  Google Scholar 

  • Wang J, Chen C (2009) Biosorbents for heavy metals removal and their future. Biotechnol Adv 27:195–226

    Article  Google Scholar 

  • Wrobel K, Escobosa ARC, Ibarra AAG et al (2015) Mechanistic insight into chromium (VI) reduction by oxalic acid in the presence of manganese (II). J Hazard Mater 300:144–152

    Article  CAS  Google Scholar 

  • Xie P, Hao X, Mohamad OA et al (2013) Comparative study of chromium biosorption by Mesorhizobium amorphae strain CCNWGS0123 in single and binary mixtures. Appl Biochem Biotechnol 169:570–587

    Article  CAS  Google Scholar 

  • Yahya SK, Zakaria ZA, Samin J et al (2012) Isotherm kinetics of Cr(III) removal by non-viable cells of Acinetobacter haemolyticus. Colloids Surf B Biointerfaces 1:362–368

    Article  Google Scholar 

  • Zawadzka AM, Crawford RL, Paszczynski AJ (2007) Pyridine-2,6-bis(thiocarboxylic acid) produced by Pseudomonas stutzeri KC reduces chromium(VI) and precipitates mercury, cadmium, lead and arsenic. Biometals 20:145–158

    Article  CAS  Google Scholar 

  • Ziagova M, Dimitriadis G, Aslanidou D et al (2007) Comparative study of Cd(II) and Cr(VI) biosorption on Staphylococcus xylosus and Pseudomonas sp. in single and binary mixtures. Bioresour Technol 98:2859–2865

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by CONACyT, México, Project CB-2014-01 registry number 239575 and by DAIP Universidad de Guanajuato, México, Project FO-DAI-05.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. F. Gutiérrez-Corona.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gutiérrez-Corona, J.F., Romo-Rodríguez, P., Santos-Escobar, F. et al. Microbial interactions with chromium: basic biological processes and applications in environmental biotechnology. World J Microbiol Biotechnol 32, 191 (2016). https://doi.org/10.1007/s11274-016-2150-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11274-016-2150-0

Keywords

Navigation