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Cr(VI) mediated hydrolysis of algae cell walls to release TOC for enhanced biotransformation of Cr(VI) by a culture of Cr(VI) reducing bacteria

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Abstract

Hexavalent chromium [Cr(VI)], the most toxic form of chromium, is frequently released into the environment from anthropogenic sources. Cr(VI) mainly occurs in the oxyanionic forms, CrO42− and Cr2O72−. It is highly oxidative and carcinogenic under chronic and subchronic exposure conditions. Conventionally, Cr(VI) pollution is remediated by reducing Cr(VI) to Cr(IIII). Cr(III) is naturally less toxic than Cr(VI) and is a 1000 times less mobile in the aquatic phase than Cr(VI). Biological reduction and detoxification of Cr(VI) are viewed as the most ecologically friendly process for remediation of Cr(VI) pollution. However, fast reduction of Cr(VI) mainly occurs under aerobic conditions in the presence of organic carbon sources. In the current research, freshwater algae are utilized as a carbon source for Cr(VI) reduction with using symbiotic bacterial cultures. The algal species, Chlamydomonas reinhardtii and Chlorococcum ellipsoideum, were tested in their ability to serve as or produce a carbon source for locally isolated bacteria to achieve reduction of Cr(VI) to Cr(III). Batch experiments were conducted under aerobic conditions at different concentrations of Cr(VI) to determine the kinetics of the biological reduction reaction. In the batch experiments, complete removal of up to 50 mg L−1 of initial Cr(VI) concentration was achieved within 24 h. At 100 mg L−1 initial Cr(VI) concentration, the system could remove 92% of the Cr(VI). Algae was found to be very sensitive to Cr(VI) toxicity. The Cr(VI) inhibited the algae growth and reduced the chlorophyll a content and by extension the algae’s ability to undergo photosynthesis.

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References

  • Abdel-Raouf N, Al-Homaidan AA, Ibraheem IBM (2012) Microalgae and wastewater treatment. Saudi J Biol Sci 19:257–275

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ahemad M (2014) Bacterial mechanisms for Cr(VI) resistance and reduction: an overview and recent advances. Folia Microbiol 59:321–332

    CAS  Google Scholar 

  • APHA (2005) Standard methods for the examination of water and wastewater. 21st edition. By Clesceri LS, Greenberg AE, Eaton AD, American Public Health Association, American Water Works Association and Water Pollution Control Federation, Washington DC

  • Arita A, Costa M (2011) Environmental agents and epigenetics. In: Tollefsbol T (ed) Handbook of epigenetics. Academic Press, NY, pp 459–476

    Google Scholar 

  • Arun N, Singh DP (2014) Chromium (VI) induced oxidative stress in halotolerant alga Dunaliella salina and D. tertiolecta isolated from Ssambhar salt lake of Rajasthan (India). Cell Mol Biol 60:90–96

    CAS  PubMed  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

    PubMed  Google Scholar 

  • Bell WH, Sakshaug E (1980) Bacterial utilization of algal extracellular products. 2. A kinetic study of natural populations. Limnol Oceanogr 25:1021–1033

    Google Scholar 

  • Bridgewater LC, Manning FC, Patierno SR (1994) Base-specific arrest of in vitro DNA replication by carcinogenic chromium: relationship to DNA interstrand crosslinking. Carcinogenesis 15:2421–2427

    CAS  PubMed  Google Scholar 

  • Bruckner CG, Bahulikar R, Rahalkar M, Schink B, Kroth PG (2008) Bacteria associated with benthic diatoms from Lake Constance: phylogeny and influences on diatom growth and secretion of extracellular polymeric substances. Appl Environ Microbiol 74:7740–7749

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bush MB (2003) Ecology of a Changing Planet, 3rd Edition. Prentice Hall, New Jersey

    Google Scholar 

  • CCAP (2015) The Culture Collection of Algae and Protozoa. Medium recipe for 3N-BBM+V (Bold Basal Medium with 3-fold Nitrogen and Vitamins; modified). https://www.ccap.ac.uk/media/documents/3N_BBM_V.pdf. Accessed 27 Mar 2017

  • Chen JM, Hao OJ (1998) Microbial chromium (VI) reduction. Crit Rev Environ Sci Technol 28:219–251

    Google Scholar 

  • Chirwa EM, Molokwane PE (2011) Biological Cr (VI) reduction: microbial diversity, kinetics and biotechnological solutions to pollution. In: Solo A (ed) Biodiversity. InTech, Riejeka, pp 75–100

    Google Scholar 

  • Cicci A, Sed G, Bravi M (2017) Potential of choline chloride-based natural deep eutectic solvents (nades) in the extraction of microalgal metabolites. Chem Eng Trans 57:61–66

    Google Scholar 

  • Coenye T, Falsen E, Vancanneyt M, Hoste B, Govan JRW, Kersters K, Vandamme P (1999) Classification of Alcaligenes faecalis-like isolates from the environment and human clinical samples as Ralstonia gilardii sp. nov. Int J Syst Bacteriol 49:405–413

    PubMed  Google Scholar 

  • Cole JJ, Likens GE, Strayer DL (1982) Photosynthetically produced dissolved organic carbon: an important carbon source for planktonic bacteria. Limnol Oceanogr 27:1080–1090

    CAS  Google Scholar 

  • Dakhama A, De la Noüe J, Lavoie MC (1993) Isolation and identification of antialgal substances produced by Pseudomonas aeruginosa. J Appl Phycol 5:297–306

    CAS  Google Scholar 

  • Dong T, Knoshaug EP, Pienkos PT, Laurens LM (2016) Lipid recovery from wet oleaginous microbial biomass for biofuel production: a critical review. Appl Energy 177:879–895

    CAS  Google Scholar 

  • EPA, US (1998) Toxicological review of hexavalent chromium. Washington, DC

  • EPA-Odessa (2005) Pump and treat and in situ chemical treatment of contaminated groundwater at the Odessa Chromium II South Plume Superfund Site Odessa, Ector County, Texas. U.S. Environmental Protection Agency

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    PubMed  Google Scholar 

  • Fujie K, Toda K, Ohtake H (1990) Bacterial reduction of toxic hexavalent chromium using a fed-batch culture of Enterobacter cloacae strain HO1. J Ferment Bioengr 69:365–367

    Google Scholar 

  • Gardiner M, Hoke DE, Egan S (2014) An ortholog of the Leptospira interrogans lipoprotein LipL32 aids in the colonization of Pseudoalteromonas tunicata to host surfaces. Front Microbiol 5:323

    PubMed  PubMed Central  Google Scholar 

  • Glauert AM (1975) Fixation, dehydration and embedding of biological specimens. No. 04; QH327, G5

  • Grima EM, Belarbi EH, Fernández FA, Medina AR, Chisti Y (2003) Recovery of microalgal biomass and metabolites: process options and economics. Biotechnol Adv 20:491–515

    Google Scholar 

  • Guo Z, Tong YW (2014) The interactions between Chlorella vulgaris and algal symbiotic bacteria under photoautotrophic and photoheterotrophic conditions. J Appl Phycol 26:1483–1492

    CAS  Google Scholar 

  • Gutiérrez-Corona JF, Romo-Rodríguez P, Santos-Escobar F, Espino-Saldana AE, Hernández-Escoto H (2016) Microbial interactions with chromium: basic biological processes and applications in environmental biotechnology. World J Microbiol Biotechnol 32:191

    PubMed  Google Scholar 

  • Hassoun EA, Stohs SJ (1995) Chromium-induced production of reactive oxygen species, DNA single-strand breaks, nitric oxide production, and lactate dehydrogenase leakage in J774A. 1 cell cultures. J Biochem Mol Toxicol 10:315–321

    CAS  Google Scholar 

  • Igboamalu T, Chirwa E (2016) Kinetic study of Cr(VI) reduction in an indigenous mixed culture of bacteria in the presence of as(III). Chem Eng Trans 49:439–444

    Google Scholar 

  • Ji RP, Lu XW, Li XN, Pu YP (2009) Biological degradation of algae and microcystins by microbial enrichment on artificial media. Ecol Eng 35:1584–1588

    Google Scholar 

  • Kalckar HM (1974) Origins of the concept oxidative phosphorylation. Mol Cell Biochem 5:55–63

    CAS  PubMed  Google Scholar 

  • Kang SY, Lee JU, Kim KW (2007) Biosorption of Cr(III) and Cr(VI) onto the cell surface of Pseudomonas aeruginosa. Biochem Eng J 36:54–58

    Google Scholar 

  • Kleinová A, Cvengrošová Z, Rimarčík J, Buzetzki E, Mikulec J, Cvengroš J (2012) Biofuels from algae. Procedia Eng 42:231–238

    Google Scholar 

  • Kothari R, Pathak VV, Kumar V, Singh DP (2012) Experimental study for growth potential of unicellular alga Chlorella pyrenoidosa on dairy waste water: an integrated approach for treatment and biofuel production. Bioresour Technol 116:466–470

    CAS  PubMed  Google Scholar 

  • Kratochvil D, Pimentel P, Volesky B (1998) Removal of trivalent and hexavalent chromium by seaweed biosorbent. Environ Sci Technol 32:2693–2698

    CAS  Google Scholar 

  • Liang Z, Liu Y, Ge F, Xu Y, Tao N, Peng F, Wong M (2013) Efficiency assessment and pH effect in removing nitrogen and phosphorus by algae-bacteria combined system of Chlorella vulgaris and Bacillus licheniformis. Chemosphere 92:1383–1389

    CAS  PubMed  Google Scholar 

  • Lloyd JR (2003) Microbial reduction of metals and radionuclides. FEMS Microbiol Rev 27:411–425

    CAS  PubMed  Google Scholar 

  • Loukidou MX, Zouboulis AI, Karapantsios TD, Matis KA (2004) Equilibrium and kinetic modeling of chromium (VI) biosorption by Aeromonas caviae. Colloids Surf A 242:93–104

    CAS  Google Scholar 

  • Macfie A, Hagan E, Zhitkovich A (2009) Mechanism of DNA− protein cross-linking by chromium. Chem Res Toxicol 23:341–347

    Google Scholar 

  • Marande W, López-García P, Moreira D (2009) Eukaryotic diversity and phylogeny using small-and large-subunit ribosomal RNA genes from environmental samples. Environ Microbiol 11:3179–3188

    PubMed  Google Scholar 

  • Miranda J, Krishnakumar G, Gonsalves R (2012) Cr6+ bioremediation efficiency of Oscillatoria laete-virens (Crouan & Crouan) Gomont and Oscillatoria trichoides Szafer: kinetics and equilibrium study. J Appl Phycol 24:1439–1454

    CAS  Google Scholar 

  • Molokwane PE, Nkhalambayausi-Chirwa EM, Meli KC (2008) Chromium (VI) reduction in activated sludge bacteria exposed to high chromium loading: Brits culture (South Africa). Water Res 42:4538–4548

    CAS  PubMed  Google Scholar 

  • Munoz R, Guieysse B (2006) Algal–bacterial processes for the treatment of hazardous contaminants: a review. Water Res 40:2799–2815

    CAS  PubMed  Google Scholar 

  • Murphy V, Hughes H, McLoughlin P (2008) Comparative study of chromium biosorption by red, green and brown seaweed biomass. Chemosphere 70:1128–1134

    CAS  PubMed  Google Scholar 

  • Nakayama T, Watanabe S, Mitsui K, Uchida H, Inouye I (1996) The phylogenetic relationship between the Chlamydomonadales and Chlorococcales inferred from 18S rDNA sequence data. Phycol Res 44:47–55

    CAS  Google Scholar 

  • Nelson YM, Lion LW, Shuler ML, Ghiorse WC (1996) Modeling oligotrophic biofilm formation and lead adsorption to biofilm components. Environ Sci Technol 30:2027–2035

    CAS  Google Scholar 

  • Ozdemir G, Ceyhan N, Ozturk T, Akirmak F, Cosar T (2004) Biosorption of chromium (VI), cadmium (II) and copper (II) by Pantoea sp. TEM18 Chem Eng J 102:249–253

    CAS  Google Scholar 

  • Pell L, Löhn S, Weinberger G, Kuchta K, Hanelt D (2017) Mild disintegration methods of microalgae–bacteria flocs from wastewater treatment. J Appl Phycol 29:843–851

    CAS  Google Scholar 

  • Pritchard DE, Singh J, Carlisle DL, Patierno SR (2000) Cyclosporin a inhibits chromium(VI)-induced apoptosis and mitochondrial cytochrome c release and restores clonogenic survival in CHO cells. Carcinogenesis 21:2027–2033

    CAS  PubMed  Google Scholar 

  • Ramanan R, Kim BH, Cho DH, Oh HM, Kim HS (2016) Algae–bacteria interactions: evolution, ecology and emerging applications. Biotechnol Adv 34:14–29

    CAS  Google Scholar 

  • Rodríguez MC, Barsanti L, Passarelli V, Evangelista V, Conforti V, Gualtieri P (2007) Effects of chromium on photosynthetic and photoreceptive apparatus of the alga Chlamydomonas reinhardtii. Environ Res 105:234–239

    PubMed  Google Scholar 

  • Şahin Y, Öztürk A (2005) Biosorption of chromium (VI) ions from aqueous solution by the bacterium Bacillus thuringiensis. Process Biochem 40:1895–1901

    Google Scholar 

  • Shen H, Wang YT (1994) Modeling hexavalent chromium reduction in Escherichia coli ATCC 33456. Biotechnol Bioeng 43:293–300

    CAS  PubMed  Google Scholar 

  • Sibi G (2016) Biosorption of chromium from electroplating and galvanizing industrial effluents under extreme conditions using Chlorella vulgaris. Green Energy Environ 1:172–177

    Google Scholar 

  • Singh J, Bridgewater LC, Patierno SR (1998a) Differential sensitivity of chromium-mediated DNA interstrand crosslinks and DNA–protein crosslinks to disruption by alkali and EDTA. Toxicol Sci 45:72–76

    CAS  PubMed  Google Scholar 

  • Singh J, McLean JA, Pritchard DE, Montaser A, Patierno SR (1998b) Sensitive quantitation of chromium-DNA adducts by inductively coupled plasma mass spectrometry with a direct injection high-efficiency nebulizer. Toxicol Sci 46:260–265

    CAS  PubMed  Google Scholar 

  • Smith WA, Apel WA, Petersen JN, Peyton BM (2002) Effect of carbon and energy source on bacterial chromate reduction. Bioremediat J 6:205–215

    CAS  Google Scholar 

  • Szymczak-Żyla M, Kowalewska G, Louda JW (2008) The influence of microorganisms on chlorophyll a degradation in the marine environment. Limnol Oceanogr 53:851–862

    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 

  • Thomas PG, Quinn PJ, Williams WP (1985) The origin of photosystem-I mediated electron transport stimulation in heat-stressed chloroplasts. Planta 167:133–139

    Google Scholar 

  • Toncheva-Panova T, Ivanova J (2000) Influence of physiological factors on the lysis effect of Cytophaga on the red microalga Rhodella reticulata. J Appl Microbiol 88:358–363

    CAS  PubMed  Google Scholar 

  • Tsou TC, Chen CL, Liu TY, Yang JL (1996) Induction of 8-hydroxydeoxyguanosine in DNA by chromium(III) plus hydrogen peroxide and its prevention by scavengers. Carcinogenesis 17:103–108

    CAS  PubMed  Google Scholar 

  • Ünal D, Işik NO, Sukatar A (2010) Effects of Chromium VI stress on green alga Ulva lactuca (L.). Turk J Biol 34:119–124

  • Vidotti A, Coelho R, Franco LM, Franco TT (2014) Miniaturized culture for heterotrophic microalgae using low cost carbon sources as a tool to isolate fast and economical strains. Chem Eng Trans 38:325–330

    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

    CAS  PubMed  Google Scholar 

  • Volland S, Lütz C, Michalke B, Lütz-Meindl U (2012) Intracellular chromium localization and cell physiological response in the unicellular alga Micrasterias. Aquat Toxicol 109:59–69

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wise JP, Leonard JC, Patierno SR (1992) Clastogenicity of lead chromate particles in hamster and human cells. Mutat Res 278:69–79

    CAS  PubMed  Google Scholar 

  • World Health Organization (2004) Guidelines for drinking-water quality: recommendations (Vol. 1). World Health Organization, Geneva

  • Xu J, Bubley GJ, Detrick B, Blankenship LJ, Patierno SR (1996) Chromium(VI) treatment of normal human lung cells results in guanine-specific DNA polymerase arrest, DNA–DNA cross-links and S-phase blockade of cell cycle. Carcinogenesis 17:1511–1517

    CAS  PubMed  Google Scholar 

  • Xue Y, Jin W, Du H, Zheng S, Sun Z, Yan W, Zhang Y (2016) Electrochemical Cr (III) oxidation and mobilization by in situ generated reactive oxygen species in alkaline solution. J Electrochem Soc 163:684–689

    Google Scholar 

  • Yewalkar SN, Dhumal KN, Sainis JK (2007) Chromium (VI)-reducing Chlorella spp. isolated from disposal sites of paper-pulp and electroplating industry. J Appl Phycol 19:459–465

    CAS  Google Scholar 

  • Zhiguo H, Fengling G, Tao S, Yuehua H, Chao H (2009) Isolation and characterization of a Cr(VI)-reduction Ochrobactrum sp. strain CSCr-3 from chromium landfill. J Hazard Mater 163:869–873

    Google Scholar 

  • Ziagova M, Dimitriadis G, Aslanidou D, Papaioannou X, Tzannetaki EL, Liakopoulou-Kyriakides M (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

    CAS  PubMed  Google Scholar 

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Funding

The authors would like to thank the University of Pretoria and the Water Utilization and Environmental Engineering Division at the University of Pretoria for the research support. The research was partially funded by the National Research Foundation (NRF) of South Africa through Grant No. CSUR180215313534 awarded to Prof Evans M. N. Chirwa of the Department of Chemical Engineering and Maria Roestorff (Grant No: 114172). Additional funding was provided by the Sedibeng Water Chair in Water Utilization Engineering in the Water Utilization Division at the University of Pretoria.

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  1. Department of Chemical Engineering, University of Pretoria, Lynnwood Road, Private bag X20 Hatfield, Pretoria, 0002, South Africa

    M. M. Roestorff & E. M. N. Chirwa

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  1. M. M. Roestorff
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Roestorff, M.M., Chirwa, E.M.N. Cr(VI) mediated hydrolysis of algae cell walls to release TOC for enhanced biotransformation of Cr(VI) by a culture of Cr(VI) reducing bacteria. J Appl Phycol 31, 3637–3649 (2019). https://doi.org/10.1007/s10811-018-1716-7

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