Abstract
Scanning confocal laser microscopy was used to directly visualize accumulation of the herbicide diclofop methyl and its breakdown products by a degradative biofilm community, cultivated in continuous-flow cell cultures. Some bacterial cells accumulated these compounds. However, most accumulation occurred in cell capsules and certain regions of the exopolymer matrix. Mass spectroscopic analysis of the biofilm material confirmed accumulation of the parent compound and its breakdown products in the biofilms. Lower molecular weight degradation products were found in the effluent, indicating mineralization of diclofop by the flow cell cultures. Grazing protozoa feeding on the biofilms nonselectively ingested cell capsules and exopolymers, suggesting direct transfer and accumulation of the contaminants in protozoa. These findings demonstrated that microbial exopolymers can play an important role in the bioaccumulation of contaminants in natural systems.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Baughman GL, Paris DF (1981) Microbial bioconcentration of pollutants from aquatic systems—a critical review. Crit Rev Microbiol 8:205–228
Baxter RM (1986) Bacterial formation of humus-like materials from polychlorinated biphenyls (PCBs). Water Pollut Res J Canada 21:1–17
Bellin CA, Rao PSC (1993) Impact of bacterial biomass on contaminant sorption and transport in a subsurface soil. Appl Environ Microbiol 59:1813–1820
Bell JP, Tsezos K (1987) Removal of hazardous organic pollutants by biomass adsorption. J WPCF 59:191–198.
Bengtsson G. (1991) Bacterial exopolymer and PHB production in fluctuating ground-water habitats. FEMS Microbiol Lett 86:15–24
Boyde A (1990) Confocal optical microscopy. In: Duke PJ, Michette AG (eds) Modern microscopies. Plenum Press, New York, pp 185–204
Brown MJ, Lester JN (1982) Role of bacterial extracellular polymers in metal uptake in pure bacterial culture and activated sludge-I. Water Res 16:1539–1560
Caldwell DE, Korber DR, Lawrence JR (1992) Confocal laser microscopy and digital image analysis in microbial ecology. In: Marshall KC (ed) Advances in microbial ecology, vol. 12. Plenum Press, New York, pp 1–67
Caldwell DE, Korber DR, Lawrence JR (1992) Imaging of bacterial cells by fluorescence exclusion using scanning confocal laser microscopy. J Microb Methods 15:249–261
Caldwell DE, Lawrence JR (1986) Growth kinetics of Pseudomonas fluorescens microcolonies within the hydrodynamic boundary layers of surface microenvironments. Microb Ecol 12:299–312
Costerton JW, Cheng K-J, Geesey GG, Ladd TI, Nickel NC, Dasgupta M, Marrie TJ (1987) Bacterial biofilms in nature and disease. Annu Rev Microbiol 41:435–464
Decho AW (1990) Microbial exopolymer secretions in ocean environments: their role(s) in food webs and marine processes. Oceanogr Mar Biol Annu Rev 28:73–153
Dudman WF (1977) The role of surface polysaccharides in natural environments. In: Sutherland IW (ed) Surface carbohydrates of the prokaryotic cell. Academic Press, London, pp 357–414
Geesey GG, Bremer PJ (1990) Applications of Fourier transform infrared spectrometry to studies of copper corrosion under bacterial biofilms. Mar Technol Soc J 24:36–43
Geller A (1979) Sorption and desorption of atrazine by three bacterial species isolated from aquatic systems. Arch Environ Contam Toxicol 8:713–720
Grimes DJ, Morrison SM (1975) Bacterial bioconcentration of chlorinated hydrocarbon insecticides from aqueous systems. Microb Ecol 2:43–59
Gossett RW, Brown DA, Young DR (1983) Predicting the bioaccumulation of organic compounds in marine organisms using octanol/water partition coefficients. Mar Pollut Bull 14:387–392
Jolley JG, Geesey GG, Hankins MW, Wright RB, Wichlacz PL (1989) Auger electron and X-ray photoelectron spectroscopic study of the biocorrosion of copper by alginic acid polysaccharide. Appl Surface Sci 37:469–480
Lawrence JR, Korber DR, Hoyle BD, Costerton JW, Caldwell DE (1991) Optical sectioning of microbial biofilms. J Bacteriol 173:6558–6567
Lawrence JR, Zanyk BN, Wolfaardt GM, Hendry MJ, Robarts RD, Caldwell DE (1993) Design and evaluation of a meso-scale model vadose zone and ground water system. Ground Water 31:446–455
Leshniowsky WO, Dugan PR, Pfister RM, Frea JI, Randles CI (1970) Aldrin: removal from lake water by flocculent bacteria. Science 169:993–994
Patrick FM, Loutit M (1976) Passage of metals in influents, through bacteria to higher organisms. Water Res 10:333–335
Reineke W, Knackmuss H-J (1984) Microbial metabolism of haloaromatics: isolation and properties of a chlorobenzene-degrading bacterium. Appl Environ Microbiol 47:395–402
Rudd T, Sterritt RM, Lester JN (1983) Mass balance of heavy metal uptake by encapsulated cultures of Klebsiella aerogenes. Microb Ecol 9:261–272
Schmidt SK, Smith R, Sheker D, Hess TF, Silverstein F, Radehaus PM (1992) Interactions of bacteria and microflagellates in sequencing batch reactors exhibiting enhanced mineralization of toxic organic chemicals. Microb Ecol 23:127–142
Sherr EB (1988) Direct use of high molecular weight polysaccharide by heterotrophic flagellates. Nature 335:348–351
Sikora FJ, McBride MB (1989) Aluminum complexation by catechol as determined by ultraviolet spectrophotometry. Environ Sci Technol 23:349–356
Smith AE (1977) Degradation of the herbicide diclorfop-methyl in Prairie soils. J Agric Food Chem 25:893–898
Strandberg GW, Starling E, Shumate II, Parrott JR (1981) Microbial cells as biosorbents for heavy metals: accumulation of uranium by Saccharomyces cerevisiae and Pseudomonas aeruginosa. Appl Environ Microbiol 41:237–245
Tsezos K, Bell JP (1988) Significance of biosorption for the hazardous organics removal efficiency of a biological reactor. Water Res 22:391–394
Tsezos K, Bell JP (1989) Comparison of the biosorption and desorption of hazardous organic pollutants by live and dead biomass. Water Res 23:561–568
Uhlinger DJ, White DC (1983) Relationship between physiological status and formation of extracellular polysaccharide glycocalyx in Pseudomonas atlantica. Appl Environ Microbiol 45:64–70
Urrutia M, Kemper M, Doyle R, Beveridge TJ (1992) The membrane-induced proton motive force influences the metal binding ability of Bacillus subtilis cell walls. Appl Environ Microbiol 58:3837–3844
Wolfaardt GM, Lawrence JR, Robarts RD, Caldwell SJ, Caldwell DE (1994) Multicellular organization in a degradative biofilm community. Appl Environ Microbiol 60:434–446
Wolfaardt GM, Lawrence JR, Robarts RD, Caldwell DE (1994) The role of interactions, sessile growth and nutrient amendments on the degradative efficiency of a microbial consortium. Can. J. Microbial 40:331–340
Author information
Authors and Affiliations
Additional information
Correspondence to: J.R. Lawrence.
Rights and permissions
About this article
Cite this article
Wolfaardt, G.M., Lawrence, J.R., Headley, J.V. et al. Microbial exopolymers provide a mechanism for bioaccumulation of contaminants. Microb Ecol 27, 279–291 (1994). https://doi.org/10.1007/BF00182411
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00182411