Abstract
The formation and activity of an As(III)-oxidising biofilm in a bioreactor, using pozzolana as bacterial growth support, was studied for the purpose of optimising fixed-bed bioreactors for bioremediation. After 60 days of continuous functioning with an As(III)-contaminated effluent, the active biofilm was found to be located mainly near the inflow rather than homogeneously distributed. Biofilm development by the CAsO1 bacterial consortium and by Thiomonas arsenivorans was then studied both on polystyrene microplates and on pozzolana. Extra-cellular polymeric substances (EPS) and yeast extract were found to enhance bacteria attachment, and yeast extract also appears to increase the kinetics of biofilm formation. Analysis of proteins, sugars, lipids and uronic acids indicate that sugars were the main EPS components. The specific As(III)-oxidase activity of T. arsenivorans was higher (by ninefold) for planktonic cells than for sessile ones and was induced by As(III). All the results suggest that the biofilm structure is a physical barrier decreasing As(III) access to sessile cells and thus to As(III)-oxidase activity induction. The efficiency of fixed-bed reactors for the bioremediation of arsenic-contaminated waters can be thus optimised by controlling different factors such as temperature and EPS addition and/or synthesis to increase biofilm density and activity.
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References
Anderson G, Williams J, Hille R (1992) The purification and characterization of arsenite oxidase from Alcaligenes faecalis, a molybdenum-containing hydroxylase. J Biol Chem 267:23674–23682
Battaglia-Brunet F, Dictor MC, Garrido F, Crouzet C, Morin D, Dekeyser K, Clarens M, Baranger P (2002) An As(III)-oxidizing bacterial population: selection, characterization, and performance in bioreactors. J Appl Microbiol 93:656–667
Battaglia-Brunet F, Dictor MC, Garrido F, Michel C, Joulian C, Bourgeois F, Baranger P, Itard Y, Morin D (2005) Remediation processes using biological As(III) oxidation. Proceedings of the 16th International Biohydrometallurgy Symposium, Cape Town, South Africa: 343–350
Battaglia-Brunet F, Joulian C, Garrido F, Dictor MC, Morin D, Coupland K, Johnson D, Hallberg K, Baranger P (2006a) Oxidation of arsenite by Thiomonas strains and characterisation of Thiomonas arsenivorans sp. Nov. Antonie van Leeuwenhoek 89:99–108
Battaglia-Brunet F, Itard Y, Garrido F, Delorme F, Crouzet C, Greffié C, Joulian C (2006b) A simple biogeochemical process removing arsenic from a mine drainage water. Geomicrobiol J 23:201–211
Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Biochem 54:484–489
Challan Belval S, Gal L, Margiewes S, Garmyn D, Piveteau P, Guzzo J (2006) Assessment of the roles of LuxS, S-ribosyl homocysteine, and autoinducer 2 in cell attachment during biofilm formation by Listeria monocytogenes EGD-e. Appl Env Microbiol 72:2644–2650
Clifford D, Ghurye G, Tripp A (1999) Development of an anion exchange process for arsenic removal from water. In: Abermathy R, Calderon R (eds) Arsenic exposure and health effect. Elsevier, The Netherlands, pp 379–387
Costerton J (1999) Introduction to biofilm. Int J Antimicrob Agents 11:217–221
Daniels L, Hanson R, Phillips J (1994) Chemical analysis. In: Gerhardt P, Murray RG, Wood WA, Krieg NR (eds) Methods for general and molecular bacteriology. American Society for Microbiology, Washington DC, pp 512–554
De Lancey Pulcini (2001) Bacterial biofilms: a review of current research. Néphrologie 22:439–441
EC (1998) European Commission Directive, 98/83/EC, related with drinking water quality intended for human consumption, Brussels, Belgium, 3/11/1998
Ellis P, Conrads T, Hille R, Kuhn P (2001) Crystal structure of the 100 KDa arsenite oxidase from Alcaligenes faecalis in two crystal forms at 1.64 Å and 2.03 Å. Structure 9:125–132
Frings C, Frendley T, Dunn R, Queen C (1972) Improved determination of total serum lipids by the sulfo-phospho-Vanillin reaction. Clin Chem 18:673–674
Gihring T, Banfield J (2001) Arsenite oxidation and arsenate respiration by a new Thermus isolate. FEMS Microbiol Lett 204:335–340
Gihring T, Druschel G, McCleskey R, Hamers R, Banfield J (2001) Rapid arsenite oxidation by Thermus aquaticus and Thermus thermophilus: field and laboratory investigations. Environ Sci Technol 35:3857–3862
Gilbert P, Collier P, Brown M (1990) Influence of growth rate on susceptibility to antimicrobial agents: biofilms, cell cycle, dormancy, and stringent response. Antimicrob Agents Chemother 34:1865–1868
Häußler S (2004) Biofilm formation by the small colony variant phenotype of Pseudomonas aeruginosa. Environ Microbiol 6:546–551
Ilyaletdonov AN, Abdrashitova SA (1981) Autotrophic oxidation of arsenic by Pseudomonas arsenitoxidans. Mikrobiologia 50:197–204
Inskeep W, Macur R, Hamamura N, Warelow T, Ward S, Santini J (2007) Detection, diversity and expression of aerobic bacterial arsenite oxidase genes. Environ Microbiol 9:934–943
Jekel MR (1994) Removal of arsenic in drinking water treatment. In: Nriagu JO (eds) Arsenic in Environment, part I: Cycling and characterization. Wiley, New York NY, pp 119–132
Laffey S, Butler G (2005) Phenotype switching affects biofilm formation by Candida papsilosis. Microbiology 151:1073–1081
Lalonde B, Girardot PL (1991) L’eau et les collectivités locales, IAURIF, Edition du Moniteur, Paris, France
Lebrun E, Brugna M, Baymann F, Muller D, Lièvremont D, Lett MC, Nitschke W (2003) Arsenite oxidase, an ancient bioenergetic enzyme. Mol Biol Evol 20:686–693
Lehman RM, O’Connell SP (2002) Comparison of extracellular enzyme activities and community composition of attached and free-living bacteria in porous medium columns. Appl Environ Microbiol 68(4):1569–1575
Lièvremont D, N’negue MA, Behra P, Lett MC (2003) Biological oxidation of arsenite: batch reactor experiments in presence of kutnahorite and chabazite. Chemosphere 51:419–428
Macur R, Jackson C, Botero L, McDermott T, Inskeep W (2004) Bacterial populations associatd with the oxidation and reduction of arsenic in an unsaturated soil. Environ Sci Technol 38:104–111
Muller D, Lièvremont D, Simeonova D, Hubert JC, Lett MC (2003) Arsenite oxidase aox genes from a metal-resistant β-proteobacterium. J Bact 185:135–141
Muller D, Simeonova DD, Riegal P, Mangenot S, Koechler S, Lièvremont D, Bertin PN, Lett MC (2006) Herminiimonas arsenicoxydans sp. nov., a metalloresistant bacterium. Int J Syst Evol Microbiol 56:1765–1769
Rhine ED, Phelps CD, Young LY (2006) Anaerobic arsenite oxidation by novel denitrifying isolates. Environ Microbiol 8:899–908
Salmassi T, Venkateswaren K, Satomi M, Nealson K, Newman D, Hering J (2002) Oxidation of arsenite by Agrobacterium albertimagni, AOL15, sp.nov., isolated from hot creek, California. Geomicrobiol J 19:53–66
Sand W, Gehrke T (1999) Analysis and function of the EPS from the strong acidophile Thiobacillus ferrooxidans. In: Wingender J, Neu T, Flemming H (eds) Microbial extracellular polymeric substances: characterisation, structure and function. Springer, New York, pp 127–141
Sand W, Gehrke T (2006) Extracellular polymeric substances mediate bioleaching/biocorrosion via interfacial processes involving iron(III) ions and acidophilic bacteria. Res Microbiol 157:49–56
Santini JM, Sly LI, Schnagl RD, Macy JM (2000) A new chemolithoautotrophic arsenite-oxidizing bacterium isolated from a gold mine: phylogenetic, physiological, and preliminary biochemical studies. Appl Environ Microbiol 66:92–97
Santini JM, Sly LI, Wen AM, Comrie D, Wulf-Durand P, Macy JM (2002) New arsenite-oxidizing bacteria isolated from Australian gold mining environments: phylogenetic relationships. Geomicrobiol J 19:67–76
Silver S, Phung L (2005) Genes and enzymes involved in bacterial oxidation and reduction of inorganic arsenic. Appl Env Microbiol 71:599–608
Stewart P (1994) Biofilm accumulation model that predicts antibiotic resistance of Pseudomonas aeruginosa biofilms. Antimicrob Agents Chemother 38:1052–1058
Suttigarn A, Wang Y-T (2005) Arsenite oxidation by Alcaligenes faecalis strain O1201. J Environ Eng 131:1293–1301
Teitzel G, Parsek M (2003) Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. App Env Micobiol 69:2313–2320
Turner AW (1954) Bacterial oxidation of arsenite. I. Description of bacteria isolated from cattle-dipping fluids. Aust J Biol Sci 7:452–478
Wakimoto N, Nishi J, Sheikh J, Nataro J, Sarantuya J, Iwashita M, Manago K, Tokuda K, Yoshinaga M, Kawano Y (2004) Quantitative biofilm assay using a microtiter plate to screen for enteroaggregative Escherichia coli. Am J Trop Med Hyg 71:687–690
Welté B (2002) L’arsenic- 4ème partie. Traitement. TSM numéro 5–97ème année. pp 36–45
Wingender J, Neu T, Flemming H (1999) What are bacterial extracellular polymeric substances? In: Wingender J, Neu T, Flemming H (eds) Microbial extracellular polymeric substances. Springer, New York, pp 1–19
Wolfaardt G, Lawence J, Korber D (1999) Function of EPS. In: Wingender J, Neu T, Flemming H (eds) Microbial extracellular polymeric substances. Springer, New York, pp 171–200
Zhan XM, Rodgers M, O’Reilly E (2006) Biofilm growth and characteristics in an alternating pumped sequencing batch biofilm reactor (APSBBR). Water Res 40:817–825
Acknowledgement
The work was carried out in the framework of the BRGM contribution to the French “Réseau National Biofilm”, Research Group GDR no. 2909 (Métabolisme de l’arsenic chez les prokaryotes: de la résistance à la détoxication) and received financial support from the BRGM Research Division (BIOPROC/Biofilm and Enzenv projects, Contribution no. 05059). Part of the work (bioreactor experiments) was also supported by the AsTHIOX RITEAU project (Decision no. 03V320). We would also like to thank Marie-Claire Lett from the University of Strasbourg (ULP, France) and Pascal Piveteau and Sylvain Challan Belval from ENSBANA, Dijon (France) for technical and scientific discussions.
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Michel, C., Jean, M., Coulon, S. et al. Biofilms of As(III)-oxidising bacteria: formation and activity studies for bioremediation process development. Appl Microbiol Biotechnol 77, 457–467 (2007). https://doi.org/10.1007/s00253-007-1169-4
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DOI: https://doi.org/10.1007/s00253-007-1169-4