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Original Articles

Sphaerotilus natans, a Neutrophilic Iron-Related Sheath-Forming Bacterium: Perspectives for Metal Remediation Strategies

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Pages 64-75 | Received 01 Mar 2013, Accepted 01 May 2013, Published online: 25 Oct 2013

References

  • Ankrah , D A and Søgaard , E G . 2009 . “ A review of biological iron removal ” . In Thirteenth International Water Technology Conference Hurgada, Egypt, March 12–15 2009, Proceedings, 3rd ed , Vol. 2 , p999 – 1005 . Zagazig : Hurghada .
  • Beolchini , F , Pagnanelli , F , Toro , L and Vegliò , F . 2003 . Biosorption of copper by Sphaerotilus natans immobilised in polysulfone matrix: equilibrium and kinetic analysis . Hydrometallurgy , 70 : 101 – 112 .
  • Beolchini , F , Pagnanelli , F , Toro , L and Vegliò , F . 2006 . Ionic strength effect on copper biosorption by Sphaerotilus natans: equilibrium study and dynamic modelling in membrane reactor . Water Res , 40 : 144 – 152 .
  • Caravelli , A H , Giannuzzi , L and Zaritzky , E . 2008 . Reduction of hexavalent chromium by Sphaerotilus natans a filamentous micro-organism present in activated sludges . Journal of Hazardous Materials , 156 : 214 – 222 .
  • Chan , C S , De Stasio , G , Welch , S A , Girasole , M , Frazer , B H , Nesterova , M V , Fakra , S and Banfield , J F . 2004 . Microbial polysaccharides template assembly of nanocrystal fibers . Science , 303 : 1656 – 1658 .
  • Chan , C S , Fakra , S C , Emerson , D , Fleming , E J and Edwards , K J . 2011 . Lithotrophic iron-oxidizing bacteria produce organic stalks to control mineral growth: implications for biosignature formation . ISME J , 5 : 717 – 727 .
  • Chaturvedi , S and Dave , P N . 2012 . Removal of iron for safe drinking water . Desalination , 303 : 1 – 11 .
  • Contreras , E M , Giannuzzi , L and Zaritzky , N E . 2000 . Growth kinetics of the microorganism Sphaerotilus natans in a model system of a food industry wastewater . Water Res , 34 : 4455 – 4463 .
  • Converti , A , Fiorito , G , Zilli , M , Lodi , A , Del Borghi , M and Ferraiolo , G . 1992 . Magnesium uptake by Sphaerotilus natans. The inhibiting effect of ethanol . Bioproc Eng , 7 : 325 – 330 .
  • Corstjens , P L , de Vrind , J P , Westbroek , P and de Vrind-de Jong , E W . 1992 . Enzymatic iron oxidation by Leptothrix discophora: identification of an iron-oxidizing protein . Appl Environ Microbiol , 58 : 450 – 454 .
  • Demoll , R and Liebmann , H . 1952 . Über die verteilung von Sphaerotilus natans in fluss . Schweizerische zeitschrift für hydrologie - Swiss J Hydrol , 17 : 112 – 125 .
  • Dias , F F and Heukelekian , H . 1967 . Utilization of inorganic nitrogen compounds by Sphaerotilus natans growing in a continuous-flow apparatus . Appl Microbiol , 15 : 1083 – 1086 .
  • Dias , F F , Okrend , H and Dondero , N C . 1968 . Calcium nutrition of Sphaerotilus growing in a continuous-flow apparatus . Appl Environ Microbiol , 16 : 1364 – 1369 .
  • Dimitrakos Michalakos , G , Martínez Nieva , J and Vayenas , D V, G L . 1997 . Removal of iron from potable water using a trickling filter . Water Res , 31 : 991 – 996 .
  • Doetsch , RN. 1966 . Notes on some structural features of Sphaerotilus natans . Arch Microbiol , 54 : 46 – 55 .
  • Dondero , NC. 1961 . Sphaerotilus, its nature and economic significance . Adv Appl Microbiol , 3 : 77 – 107 .
  • Dondero , NC. 1975 . The Sphaerotilus-Leptothrix group . Ann Rev Microbiol , 29 : 407 – 428 .
  • Druschel , G K , Emerson , D , Sutka , R , Suchecki , P and Luther , G W III . 2008 . Low-oxygen and chemical kinetic constraints on the geochemical niche of neutrophilic iron(II) oxidizing microorganisms . Geochim Cosmochim Acta , 72 : 3358 – 3370 .
  • Duckworth , O W , Holmström , S JM , Peña , J and Sposito , G . 2009 . Biogeochemistry of iron oxidation in a circumneutral freshwater habitat . Chem Geol , 260 : 149 – 158 .
  • Eikelboom , DH. 1975 . Filamentous organisms observed in activated sludge . Water Res , 9 : 365 – 388 .
  • Emerson , D , Fleming , E J and McBeth , J M . 2010 . Iron-oxidizing bacteria: an environmental and genomic perspective . Ann Rev Microbiol , 64 : 561 – 583 .
  • Emerson , D and Moyer , C . 1997 . Isolation and characterization of novel iron-oxidizing bacteria that grow at circumneutral pH . Appl Environ Microbiol , 63 : 4784 – 4792 .
  • Esposito , A , Pagnanelli , F , Lodi , A , Solisio , C and Vegliò , F . 2001 . Biosorption of heavy metals by Sphaerotilus natans: an equilibrium study at different pH and biomass concentrations . Hydrometallurgy , 60 : 129 – 141 .
  • Esposito , A , Pagnanelli , F and Vegliò , F . 2002 . pH-related equilibria models for biosorption in single metal systems . Chem Eng Sci , 57 : 307 – 313 .
  • Ferris , F. 2005 . Biogeochemical properties of bacteriogenic iron oxides . Geomicrobiol J , 22 : 79 – 85 .
  • Ferris , F , Hallberg , R , Lyvén , B and Pedersen , K . 2000 . Retention of strontium, cesium, lead and uranium by bacterial iron oxides from a subterranean environment . Appl Geochem , 15 : 1035 – 1042 .
  • Fleming , E J , Langdon , A E , Martinez-Garcia , M , Stepanauskas , R , Poulton , N J , Masland , EDP and Emerson , D . 2011 . What's new is old: resolving the identity of Leptothrix ochracea using single cell genomics, pyrosequencing and FISH . PloS one , 6 : e17769
  • Fortin , D and Langley , S . 2005 . Formation and occurrence of biogenic iron-rich minerals . Earth-Sci Rev , 72 : 1 – 19 .
  • Gadd , GM. 2004 . Microbial influence on metal mobility and application for bioremediation . Geoderma , 122 : 109 – 119 .
  • Gaudy , E and Wolfe , R S . 1961 . Factors affecting filamentous growth of Sphaerotilus natans . Appl Microbiol , 9 : 580 – 584 .
  • Gault , A G , Ibrahim , A , Langley , S , Renaud , R , Takahashi , Y , Boothman , C , Lloyd , J R , Clark , I D , Ferris , F G and Fortin , D . 2011 . Microbial and geochemical features suggest iron redox cycling within bacteriogenic iron oxide-rich sediments . Chem Geol , 281 : 41 – 51 .
  • Gault , A G , Langley , S , Ibrahim , A , Renaud , R , Takahashi , Y , Boothman , C , Lloyd , J R , Clark , I D , Ferris , F G and Fortin , D . 2012 . Seasonal changes in mineralogy, geochemistry and microbial community of bacteriogenic iron oxides (BIOS) deposited in a circumneutral wetland . Geomicrobiol J , 29 : 161 – 172 .
  • Gaval , G and Pernelle , J-J . 2003 . Impact of the repetition of oxygen deficiencies on the filamentous bacteria proliferation in activated sludge . Water Res , 37 : 1991 – 2000 .
  • Gridneva , E , Chernousova , E , Dubinina , G , Akimov , V , Kuever , J , Detkova , E and Grabovich , M . 2011 . Taxonomic investigation of representatives of the genus Sphaerotilus: descriptions of Sphaerotilus montanus sp. nov., Sphaerotilus hippei sp. nov., Sphaerotilus natans subsp. natans subsp. nov. and Sphaerotilus natans subsp. sulfidivorans subsp. nov., and an emended description of the genus Sphaerotilus . Inter J System Evolution Microbiol , 61 : 916 – 925 .
  • Gridneva , E V , Grabovich , M Y , Dubinina , G A , Chernousova , E Y and Akimov , V N . 2009 . Ecophysiology of lithotrophic sulfur-oxidizing Sphaerotilus species from sulfide springs in the Northern Caucasus . Microbiology , 78 : 76 – 83 .
  • Hallberg , R and Ferris , F G . 2004 . Biomineralization by Gallionella . Geomicrobiol J , 21 : 325 – 330 .
  • Hallbeck , L and Pedersen , K . 1991 . Autotrophic and mixotrophic growth of Gallionella ferruginea . J Gen Microbiol , 137 : 2657 – 2661 .
  • Hallbeck , L , Ståhl , F and Pedersen , K . 1993 . Phylogeny and phenotypic characterization of the stalk-forming and iron-oxidizing bacterium Gallionella ferruginea . J Gen Microbiol , 139 : 1531 – 1535 .
  • Hashim , M A , Mukhopadhyay , S , Sahu , J N and Sengupta , B . 2011 . Remediation technologies for heavy metal contaminated groundwater . J Environ Mgmt , 92 : 2355 – 2388 .
  • Hedrich , S , Schlömann , M and Johnson , D B . 2011 . The iron-oxidizing proteobacteria . Microbiology , 157 : 1551 – 1564 .
  • James , R and Ferris , F . 2004 . Evidence for microbial-mediated iron oxidation at a neutrophilic groundwater spring . Chem Geol , 212 : 301 – 311 .
  • Jensen , E C , Schrader , H S , Rieland , B , Thompson , T L , Lee , KITW , Nickerson , K W and Kokjohn , T A . 1998 . Prevalence of broad-host-range lytic bacteriophages of Sphaerotilus natans, Escherichia coli, and Pseudomonas aeruginosa . Appl Environ Microbiol , 64 : 575 – 580 .
  • Kämpfer , P. 1998 . Some chemotaxonomic and physiological properties of the genus Sphaerotilus . System Appl Microbiol , 21 : 245 – 250 .
  • Katsoyiannis , IA. 2007 . Carbonate effects and pH-dependence of uranium sorption onto bacteriogenic iron oxides: kinetic and equilibrium studies . J Hazard Mater , 139 : 31 – 37 .
  • Katsoyiannis , I A , Werner , H , Bartel , H and Jekel , M . 2006 . The effect of groundwater composition on uranium (VI) sorption onto bacteriogenic iron oxides . Water Res , 40 : 3646 – 3652 .
  • Katsoyiannis , I A and Zouboulis , A I . 2002 . Removal of arsenic from contaminated water sources by sorption onto iron-oxide-coated polymeric materials . Water Res , 36 : 5141 – 5155 .
  • Katsoyiannis , I A and Zouboulis , A I . 2004 . Biological treatment of Mn (II) and Fe (II) containing groundwater: kinetic considerations and product characterization . Water Res , 38 : 1922 – 1932 .
  • Keim , CN. 2011 . Arsenic in biogenic iron minerals from a contaminated environment . Geomicrobiol J , 28 : 242 – 251 .
  • Kennedy , C B , Gault , A G , Fortin , D , Clark , I D and Ferris , F G . 2011 . Retention of iodide by bacteriogenic iron oxides . Geomicrobiol J , 28 : 387 – 395 .
  • Klueglein , N and Kappler , A . 2013 . Abiotic oxidation of Fe(II) by reactive nitrogen species in cultures of the nitrate-reducing Fe(II) oxidizer Acidovorax sp. BoFeN1 – questioning the existence of enzymatic Fe(II) oxidation . Geobiology , 11 : 180 – 190 .
  • Kondo , K , Takeda , M , Ejimaa , W , Kawasaki , Y , Umezua , T , Yamada , M , Koizumi , J , Mashima , T and Katahirab , M . 2011 . Study of a novel glycoconjugate, thiopeptidoglycan, and a novel polysaccharide lyase, thiopeptidoglycan lyase . Inter J Biol Macromol , 48 : 256 – 262 .
  • Kondo , K , Takeda , M , Mashima , T , Katahira , M , Koizumi , J and Ueda , K . 2012 . Conformational analysis of an extracellular polysaccharide produced by Sphaerotilus natans . Carbohydr Res , 360 : 102 – 108 .
  • Konhauser , K. 2007 . Introduction to Geomicrobiology. , Padstow : John Wiley & Sons .
  • Konhauser , KO. 1998 . Diversity of bacterial iron mineralization . Earth-Science Reviews , 43 : 91 – 121 .
  • Kützing , FT. 1833 . Sphaerotilus natans, eine neue Süsswasseralge . Linnaea , 8 : 385 – 387 .
  • Langley , S , Gault , A G , Ibrahim , A , Takahashi , Y , Renaud , R , Fortin , D , Clark , I D and Ferris , F G . 2009 . Sorption of strontium onto bacteriogenic iron oxides . Environ Sci Technol , 43 : 1008 – 1014 .
  • Lodi , A , Solisio , C , Converti , A and Del Borghi , M . 1998 . Cadmium, zinc, copper, silver and chromium (III) removal from wastewaters by Sphaerotilus natans . Bioproc Eng , 19 : 197 – 203 .
  • Madigan , M T , Martinko , J M , Stahl , D and Clark , D P . 2012 . Brock Biology of Microorganisms. 13th Edition , San Francisco : Pearson Education, Inc .
  • Martinez , R E and Ferris , F G . 2005 . Review of the surface chemical heterogeneity of bacteriogenic iron oxides: proton and cadmium sorption . Amer J Sci , 305 : 854 – 871 .
  • Martinez , R E , Pedersen , K and Ferris , F G . 2004 . Cadmium complexation by bacteriogenic iron oxides from a subterranean environment . J Coll Interf Sci , 275 : 82 – 89 .
  • Miot , J , Benzerara , K , Morin , G , Kappler , A , Bernard , S , Obst , M , Férard , C , Skouri-Panet , F , Guigner , J-M and Posth , N . 2009 . Iron biomineralization by anaerobic neutrophilic iron-oxidizing bacteria . Geochim Cosmochim Acta , 73 : 696 – 711 .
  • Mulder , E G and van Veen , W L . 1963 . Investigations on the Sphaerotilus-Leptothrix group . Anton van Leeuwen , 29 : 121 – 153 .
  • Okrend , H and Dondero , N C . 1964 . Requirement of Sphaerotilus for cyanocobalamin . J Bacteriol , 87 : 286 – 292 .
  • Pacini , V A , María Ingallinella , A and Sanguinetti , G . 2005 . Removal of iron and manganese using biological roughing up flow filtration technology . Water Res , 39 : 4463 – 4475 .
  • Pagnanelli , F , Beolchini , F , Di Biase , A and Vegliò , F . 2004 . Biosorption of binary heavy metal systems onto Sphaerotilus natans cells confined in an UF/MF membrane reactor: dynamic simulations by different Langmuir-type competitive models . Water Res , 38 : 1055 – 1061 .
  • Pagnanelli , F , Esposito , A , Toro , L and Vegliò , F . 2003 . Metal speciation and pH effect on Pb, Cu, Zn and Cd biosorption onto Sphaerotilus natans: Langmuir-type empirical model . Water Res , 37 : 627 – 633 .
  • Pagnanelli , F , Esposito , A and Vegliò , F . 2002 . Multi-metallic modelling for biosorption of binary systems . Water Res , 36 : 4095 – 4105 .
  • Pellegrin , V , Juretschko , S , Wagner , M and Cottenceau , G . 1999 . Morphological and biochemical properties of a Sphaerotilus sp. isolated from paper mill slimes . Appl Environ Microbiol , 65 : 156 – 162 .
  • Phaup , JD. 1968 . The biology of Sphaerotilus species . Water Res , 2 : 597 – 614 .
  • Pokhrel , D and Viraraghavan , T . 2006 . Arsenic removal from aqueous solution by iron oxide-coated fungal biomass: a factorial design analysis . Water Air Soil Poll , 173 : 195 – 208 .
  • Pringsheim , EG. 1949 . The filamentous bacteria Sphaerotilus, Leptothrix, Cladothrix, and their relation to iron and manganese . Phil Trans Royal Soc B: Biol Sci , 233 : 453 – 482 .
  • Qin , S , Ma , F , Huang , P and Yang , J . 2009 . Fe (II) and Mn (II) removal from drilled well water: a case study from a biological treatment unit in Harbin . Desalination , 245 : 183 – 193 .
  • Rentz , J A , Kraiya , C , Luther , G W III and Emerson , D . 2007 . Control of ferrous iron oxidation within circumneutral microbial iron mats by cellular activity and autocatalysis . Environ Sci Technol , 41 : 6084 – 6089 .
  • Romano , A H and Geason , D J . 1964 . Pattern of sheath synthesis in Sphaerotilus natans . J Bacteriol , 88 : 1145 – 1150 .
  • Rossetti , S , Tomei , M C , Nielsen , P H and Tandoi , V . 2005 . “Microthrix parvicella”, a filamentous bacterium causing bulking and foaming in activated sludge systems: a review of current knowledge . FEMS Microbiol Rev , 29 : 49 – 64 .
  • Sharma , S K , Petrusevski , B and Schippers , J C . 2005 . Biological iron removal from groundwater: a review . J Water Supp Res Technol , 54 : 239 – 247 .
  • Shopska , M , Cherkezova-Zheleva , Z P , Paneva , D G , Iliev , M , Kadinov , G B , Mitov , I G and Groudeva , V I . 2013 . Biogenic iron compounds: XRD, Mossbauer and FTIR study . Cent Euro J Chem , 11 : 215 – 227 .
  • Siering , P L and Ghiorse , W C . 1996 . Phylogeny of the Sphaerotilus-Leptothrix group inferred from morphological comparisons, genomic fingerprinting, and 16S ribosomal DNA sequence analyses . Inter J System Bacteriol , 46 : 173 – 182 .
  • Small , T D , Warren , L A and Ferris , F G . 2001 . Influence of ionic strength on strontium sorption to bacteria, Fe(III) oxide, and composite bacteria-Fe(III) oxide surfaces . Appl Geochem , 16 : 939 – 946 .
  • Sobolev , D and Roden , E E . 2001 . Suboxic deposition of ferric iron by bacteria in opposing gradients of Fe (II) and oxygen at circumneutral pH . Appl Environ Microbiol , 67 : 1328 – 1334 .
  • Sommaruga , R and Psenner , R . 1995 . Permanent presence of grazing-resistant bacteria in a hypertrophic lake . Appl Environ Microbiol , 61 : 3457 – 3459 .
  • Spring , S. 2006 . “ The genera Leptothrix and Sphaerotilus ” . In The Prokaryotes , Edited by: Dworkin , M , Falkow , S , Rosenberg , E , Schleifer , K-H and Stackebrandt , E . Vol. 5 , 758 – 777 . New York : Springer .
  • Stokes , JL. 1953 . Studies on the filamentous sheathed iron bacterium Sphaerotilus natans . J Bacteriol , 67 : 278 – 291 .
  • Straub , K , Benz , M and Schink , B . 2001 . Iron metabolism in anoxic environments at near neutral pH . FEMS Microbiol Ecol , 34 : 181 – 186 .
  • Suzuki , T , Kanagawa , T and Kamagata , Y . 2002 . Identification of a gene essential for sheathed structure formation in Sphaerotilus natans, a filamentous sheathed bacterium . Appl Environ Microbiol , 68 : 365 – 371 .
  • Szewzyk , U , Szewzyk , R , Schmidt , B and Braun , B . 2011 . “ Neutrophilic iron-depositing microorganisms ” . In Biofilm Highlights. Springer Series on Biofilm 5 , Edited by: Flemming , H-C , Wingender , J and Szewzyk , U . p63 – 79 . Berlin Heidelberg : Springer-Verlag .
  • Takeda , M , Iohara , K , Shinmaru , S , Suzuki , I and Koizumi , J-I . 2000 . Purification and properties of an enzyme capable of degrading the sheath of Sphaerotilus natans . Appl Environ Microbiol , 66 : 4998 – 5004 .
  • Takeda , M , Matsuoka , H , Hamana , H and Hikuma , M . 1995 . Biosynthesis of poly-3-hydroxybutyrate by Sphaerotilus natans . Appl Microbiol Biotechnol , 43 : 31 – 34 .
  • Takeda , M , Miyanoiri , Y , Nogami , T , Oda , K , Saito , T , Kato , K , Koizumi , J and Katahira , M . 2007 . Structural analysis of the fundamental polymer of the sheath constructed by Sphaerotilus natans . Biosci Biotechnol Biochem , 71 : 2992 – 2998 .
  • Takeda , M , Nishina , K , Hanaoka , Y , Higo , M , Terui , M , Suzuki , I and Koizumi , J . 2003 . A novel gene encoding an enzyme that degrades a polysaccharide from the sheath of Sphaerotilus natans . Biosci Biotechnol Biochem , 67 : 2300 – 2303 .
  • Takeda , M , Nakano , F , Nagase , T , Iohara , K and Koizumi , J . 1998 . Isolation and chemical composition of the sheath of Sphaerotilus natans . Biosci Biotechnol Biochem , 62 : 1138 – 1143 .
  • Takeda , M , Nomoto , S and Koizumi , J . 2002 . Structural analysis of the extracellular polysaccharide produced by Sphaerotilus natans . Biosci Biotechnol Biochem , 66 : 1546 – 1551 .
  • Takeda , M , Suzuki , I and Koizumi , J . 2005 . Paenibacillus hodogayensis sp. nov., capable of degrading the polysaccharide produced by Sphaerotilus natans . Inter J System Evolution Microbiol , 55 : 737 – 741 .
  • Takeda , M , Umezu , T , Kawasaki , Y , Shimura , S , Kondo , K and Koizumi , J . 2012 . A spatial relationship between sheath elongation and cell proliferation in Sphaerotilus natans . Bioscience, Biotechnol Biochem , 76 : 2357 – 2359 .
  • Vasconcelos , MTSD , Leal , M FC and van den Berg , C MG . 2002 . Influence of the nature of the exudates released by different marine algae on the growth, trace metal uptake and exudation of Emiliania huxleyi in natural seawater . Mar Chem , 77 : 187 – 210 .
  • Van Veen , W L , Mulder , E G and Deinema , M H . 1978 . The Sphaerotilus-Leptothrix group of bacteria . Microbiol Rev , 42 : 329 – 356 .
  • Venosa , AD. 1975 . Lysis of Sphaerotilus natans swarm cells by Bdellovibrio bacteriovorus . Appl Microbiol , 29 : 702 – 705 .
  • De Vet , WWJM , Dinkla , I JT , Rietveld , L C and Van Loosdrecht , M CM . 2011 . Biological iron oxidation by Gallionella spp. in drinking water production under fully aerated conditions . Water research , 45 : 5389 – 5398 .
  • Vijayaraghavan , K and Yun , Y-S . 2008 . Bacterial biosorbents and biosorption . Biotechnol Adv , 26 : 266 – 291 .
  • Vollrath , S , Behrends , T and Van Cappellen , P . 2012 . Oxygen dependency of neutrophilic Fe(II) oxidation by Leptothrix differs from abiotic reaction . Geomicrobiol J , 29 : 550 – 560 .
  • De Vrind-de Jong , E W , Corstjens , P L , Kempers , E S , Westbroek , P and de Vrind , J P . 1990 . Oxidation of manganese and iron by Leptothrix discophora: use of N,N,N′,N′-Tetramethyl-p-Phenylenediamine as an indicator of metal oxidation . Appl Environ Microbiol , 56 : 3458 – 3462 .
  • Winogradsky , S. 1888 . Über eisenbakterien . Botanische Zeitung , 46 : 262 – 70 .
  • Winston , V and Thompson , T L . 1979 . Isolation and characterization of a bacteriophage specific for Sphaerotilus natans which contain an unusual base in its deoxyribonucleic acid . Appl Environ Microbiol , 37 : 1025 – 1030 .
  • Yoshikawa , H and Takiguchi , Y . 1979 . Attached growth of Sphaerotilus natans in continuous-flow apparatus and its growth inhibition by 9-beta-D-Arabinofuranosyladenine . Appl Environ Microbiol , 38 : 200 – 204 .
  • Zhang , W , Cai , J and Zhang , D . 2012 . Preparation and properties of ferrite derived from iron oxidizing bacteria . Chin Sci Bull , 57 : 2470 – 2474 .
  • Zhao , J , Guan , X and Unuma , H . 2007 . Preparation of Fe3O4 nanoparticles and their application to composite biosorbent . J Ceram Soc Japan , 115 : 475 – 478 .
  • Zhu , J , Huang , Q , Pigna , M and Violante , A . 2012 . Competitive sorption of Cu and Cr on goethite and goethite–bacteria complex . Chem Eng J , 179 : 26 – 32 .

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