Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-25T22:14:05.810Z Has data issue: false hasContentIssue false
  • English
  • Français

Spatial Architecture of Nitrifying Bacteria Biofilm Immobilized on Polyurethane Foam in an Automatic Biodetector for Water Toxicity

Published online by Cambridge University Press:  02 September 2010

Andrzej Woznica ,
Jagna Karcz ,
Agnieszka Nowak ,
Aleksander Gmur  and
Tytus Bernas
Andrzej Woznica*
Affiliation:
Department of Biochemistry, Faculty of Biology and Environmental Protection, University of Silesia, 40-032 Katowice, Poland,
Jagna Karcz
Affiliation:
Laboratory of Scanning Electron Microscopy, Faculty of Biology and Environmental Protection, University of Silesia, 40-032 Katowice, Poland,
Agnieszka Nowak
Affiliation:
Department of Biochemistry, Faculty of Biology and Environmental Protection, University of Silesia, 40-032 Katowice, Poland,
Aleksander Gmur
Affiliation:
Department of Radiology, District Hospital, 43-200 Pszczyna, Poland
Tytus Bernas
Affiliation:
Department of Plant Anatomy & Cytology, Faculty of Biology and Environmental Protection, University of Silesia, 40-032 Katowice, Poland Department of Physiology and Medical Physics, RCSI, Dublin 2, Ireland
*
Corresponding author. E-mail: [email protected]
Get access

Abstract

We describe the architecture of nitrifying bacteria biofilms immobilized on a three-dimensional (3D) polyurethane foam that permits efficient water flow through a bioreactor. The 3D spatial organization of immobilized bacterial colonies is characterized on three resolution levels with X-ray tomography, light confocal microscopy, and scanning electron microscopy (SEM). Using these techniques we demonstrate biofilm distribution in the foam and the existence of several modes of binding of bacteria to the foam. Computed X-ray tomography permits observation of the distribution of the biofilm in the whole open cellular polyurethane material volume and estimation of biofilm volume. SEM and confocal laser scanning microscopy techniques permit 3D visualization of biofilm structure. Three distinct immobilization patterns could be observed in the open cellular polyurethane material: (1) large irregular aggregates of bacterial biofilm that exist as irregular biofilm fragments, rope-like structures, or biofilm layers on the foam surface; (2) spherical (pom-pom) aggregates of bacteria localized on the external surface of biofilm; and (3) biofilm threads adherent to the surface of polyurethane foam. Finally, we demonstrate that immobilized bacteria exhibit metabolic activity and growth.

Keywords

biofilmnitrifying bacteriaCLSMSEMX-ray computed tomographyimage processing visualization
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 16 , Issue 5 , October 2010 , pp. 550 - 560
Copyright
Copyright © Microscopy Society of America 2010

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Al-Raoush, R.I. & Willson, C.S. (2005). Extraction of physically realistic pore network properties from three-dimensional synchrotron X-ray microtomography images of unconsolidated porous media systems. J Hydrol 300, 44–64.CrossRefGoogle Scholar
Barnes, L.M., Lo, M.F., Adams, M.R. & Chamberlain, A.H.L. (1999). Effect of milk proteins on adhesion of bacteria to stainless steel surfaces. Appl Environ Microb 61, 4543–4548.CrossRefGoogle Scholar
Bothe, H., Jost, G., Schloter, M., Ward, B.B. & Witzel, K-P. (2000). Molecular analysis of ammonia oxidation and denitrification in natural environments. FEMS Microbiol Rev 24, 673–690.CrossRefGoogle ScholarPubMed
Coskuner, G., Ballinger, S.J., Davenport, R.J., Pickering, R.L., Solera, R., Head, I.M. & Curtis, T.P. (2005). Agreement between theory and measurement in quantification of ammonia-oxidizing bacteria. Appl Environ Microb 71, 6325–6334.CrossRefGoogle ScholarPubMed
Daims, H., Brühl, A., Amann, R., Schleifer, K.-H. & Wagner, M. (1999). The domain-specific probe EUB338 is insufficient for the detection of all bacteria: Development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22, 434–444.CrossRefGoogle ScholarPubMed
Daims, H., Nielsen, J.L., Nielsen, P.H., Schleifer, K-H. & Wagner, M. (2001). In situ characterization of Nitrospira-like nitrite-oxidizing bacteria active in wastewater treatment plants. Appl Environ Microb 67, 5273–5284.CrossRefGoogle ScholarPubMed
Delatolla, R., Tufenkji, N., Comeau, Y., Lamarre, D., Gadbois, A. & Berk, D. (2009). In situ characterization of nitrifying biofilm: Minimizing biomass loss and preserving perspective. Water Res 43, 1775–1787.CrossRefGoogle ScholarPubMed
Dogsa, I., Kriechbaum, M., Stopar, D. & Laggner, P. (2005). Structure of bacterial extracellular polymeric substances at different pH values as determined by SAXS. Biophys J 89, 2711–2720.CrossRefGoogle ScholarPubMed
Eisenmann, H., Letsiou, I., Feuchtinger, A., Beisker, W.O., Mannweiler, E., Hutzler, P. & Arnz, P. (2001). Interception of small particles by flocculent structures, sessile ciliates, and the basic layer of a wastewater biofilm. Appl Environ Microb 67, 4286–4292.CrossRefGoogle ScholarPubMed
Flint, S.H., Brooks, J.D. & Bremer, P.J. (2000). Properties of the stainless steel substrate, influencing the adhesion of thermo-resistant streptococci. J Food Eng 43, 235–242.CrossRefGoogle Scholar
Fratesi, S.E., Lynch, F.L., Kirkland, B.L. & Brown, L.R. (2004). Effects of SEM preparation on the appearance of bacteria and biofilms in the carter sandstone. J Sediment Res 74, 858–867.CrossRefGoogle Scholar
Garny, K., Horn, H. & Neu, T.R. (2008). Interaction between biofilm development, structure and detachment in rotating annular reactors. Bioproc Biosyst Eng 31, 619–629.CrossRefGoogle ScholarPubMed
Gieseke, A., Purkhold, U., Wagner, M., Amann, R. & Schramm, A. (2003). Structure and activity of multiple nitrifying bacteria population coexisting in a biofilm. Environ Microbiol 5, 355–369.CrossRefGoogle Scholar
Gieseke, A., Tarre, S., Green, M. & de Beer, D. (2006). Nitrification in a biofilm at low pH values: Role of in situ microenvironments and acid tolerance. Appl Environ Microb 72, 4283–4292.CrossRefGoogle Scholar
Ivanov, V., Stabnikova, O., Sihanonth, P. & Menasveta, P. (2006). Aggregation of ammonia-oxidizing bacteria in microbial biofilm on oyster shell surface World J Microb Biot 22, 807–812.CrossRefGoogle Scholar
Jahn, A.P. & Nielsen, H. (1995). Extraction of extracellular polymeric substances (EPS) from biofilm using a cation exchange resin. Water Sci Technol 32, 157–164.CrossRefGoogle Scholar
Jensen, K., Sloth, N.P., Risgaard-Petersen, N., Rysgaard, S. & Revsbech, N.P. (1994). Estimation of nitrification and denitrification from microprofiles of oxygen and nitrate in model sediment systems. Appl Environ Microb 60, 2094–2100.CrossRefGoogle ScholarPubMed
Jetten, M.S.M. (2008). The microbial nitrogen cycle. Environ Microbiol 10, 2903–2909.CrossRefGoogle ScholarPubMed
Jorand, F., Boue-Bigne, F., Block, J.C. & Urbain, V. (1998). Hydrophobic/hydrophilic properties of activated sludge exopolymeric substances. Water Sci Technol 37, 307–315.CrossRefGoogle Scholar
Jorand, F., Zartarian, F., Thomas, F., Block, J.C., Bottero, J.Y., Villemin, G., Urbain, V. & Manem, J. (1995). Chemical and structural (2D) linkage between bacteria within activated sludge flocs. Water Res 29, 1639–1647.CrossRefGoogle Scholar
Koenneke, M., Bernhard, A.E., de la Torre, J.R., Walker, C.B., Waterbury, J.B. & Stahl, D.A. (2005). Isolation of an autotrophic ammonia-oxidizing marine archaeon. Nature 437, 543–546.CrossRefGoogle Scholar
Lawrence, J.R., Korber, D.R., Hoyle, B.D., Costerton, J.W. & Caldwell, D.E. (1991). Optical sectioning of microbial biofilms. J Bacteriol 173, 6558–6567.CrossRefGoogle ScholarPubMed
Lee, L.Y., Ong, S.L. & Ng, W.J. (2004). Biofilm morphology and nitrification activities: Recovery of nitrifying biofilm particles covered with heterotrophic outgrowth. Bioresource Technol 95, 209–214.CrossRefGoogle ScholarPubMed
Leis, A.P., Schlicher, S., Franke, H. & Strathmann, M. (2005). Optically transparent porous medium for nondestructive studies of microbial biofilm architecture and transport dynamics. Appl Environ Microb 71, 4801–4808.CrossRefGoogle ScholarPubMed
Lemaire, R., Webb, R.I. & Yuan, Z. (2008). Micro-scale observation of the structure of aerobic microbial granules used for the treatment of nutrient-rich industrial wastewater. ISME J 2, 528–541.CrossRefGoogle ScholarPubMed
Ludwig, W., Strunk, O., Westram, R., Richter, L., Meier, H., Yadhumakar, , Buchner, A., Lai, T., Steppi, S., Jobb, G., Förster, W., Brettske, I., Gerber, S., Ginhart, A., Gross, O., Grumann, S., Hermann, S., Jost, R., König, A., Liss, T., Lümann, R., May, M., Nonhoff, B., Reichel, B., Strehlow, R., Stamatakis, A., Stuckmann, N., Vilbig, A., Lenke, M., Ludwig, T., Bode, A. & Schleifer, K.-H. (2004). ARB: A software environment for sequence data. Nucleic Acids Res 32, 1363–1371.CrossRefGoogle ScholarPubMed
Martiny, A.C., Jørgensen, T.M., Albrechtsen, H.J., Arvin, E. & Molin, S. (2003). Long-term succession of structure and diversity of a biofilm formed in a model drinking water distribution system. Appl Environ Microb 69, 6899–6907.CrossRefGoogle Scholar
Massol-Deya, A.A., Whallon, J., Hickey, R.F. & Tiedje, J.M. (1995). Channel structures in aerobic biofilms of fixed-film reactors treating contaminated groundwater. Appl Environ Microb 61, 769–777.CrossRefGoogle ScholarPubMed
Matsumoto, S., Terada, A., Aoi, Y., Tsuneda, S., Alpkvist, E., Picioreanu, C. & van Loosdrecht, M.C.M. (2007). Experimental and simulation analysis of community structure of nitrifying bacteria in a membrane-aerated biofilm. Water Sci Technol 55, 283–290.CrossRefGoogle Scholar
Mshandete, A.M., Björnsson, L., Kivaisi, K.A., Rubindamayugi, M.S.T. & Mattiasson, B. (2008). Performance of biofilm carriers in anaerobic digestion of sisal leaf waste leachate. Electron J Biotechnol 11, 1–8.CrossRefGoogle Scholar
Nielsen, P.H., Jahn, A. & Palmgren, R. (1997). Conceptual model for production and composition of exopolymers in biofilm. Water Sci Technol 36, 11–19.CrossRefGoogle Scholar
Okabe, S., Satoh, H. & Watanabe, Y. (1999). In situ analysis of nitrifying biofilms as determined by in situ hybridization and the use of microelectrodes. Appl Environ Microb 65, 3182–3191.CrossRefGoogle ScholarPubMed
Park, H.-D. & Noguera, D.R. (2007). Characterization of two ammonia-oxidizing bacteria isolated from reactors operated with low dissolved oxygen concentrations. J Appl Microbiol 102, 1401–1417.CrossRefGoogle ScholarPubMed
Picioreanu, C., Kreft, J-U., Klausen, M., Haagensen, J.A.J., Tolker-Nielsen, T. & Molin, S. (2007). Microbial motility involvement in biofilm structure formation—A 3D modelling study. Water Sci Technol 55, 337–343.CrossRefGoogle ScholarPubMed
Picioreanu, C., Kreft, J-U. & van Loosdrecht, M.C.M. (2004). Particle-based multidimensional multispecies biofilm model. Appl Environ Microb 70, 3024–3040.CrossRefGoogle ScholarPubMed
Priester, J.H., Horst, A.M., van de Werfhorst, L.C., Saleta, J.L., Mertes, L.A.K. & Holden, P.A. (2007). Enhanced visualization of microbial biofilms by staining and environmental scanning electron microscopy. J Microbiol Meth 68, 577–587.CrossRefGoogle ScholarPubMed
Prosser, J.I. & Nicol, G.W. (2008). Relative contributions of archaea and bacteria to aerobic ammonia oxidation in the environment. Environ Microbiol 10, 2931–2941.CrossRefGoogle ScholarPubMed
Pruesse, E., Quast, C., Knittel, K., Fuchs, B., Ludwig, W., Peplies, J. & Glöckner, F.O. (2007). SILVA: A comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nuceic Acids Res 21, 7188–7196.CrossRefGoogle Scholar
Pynaert, K., Smets, B.F., Wyffels, S., Beheydt, D., Siciliano, S.D. & Verstraete, W. (2003). Characterization of an autotrophic nitrogen-removing biofilm from a highly loaded lab-scale rotating biological contactor. Appl Environ Microb 69, 3626–3635.CrossRefGoogle ScholarPubMed
Ribeiro, R., Varesche, M.B.A., Foresti, E. & Zaiat, M. (2003). Influence of extracellular polymeric substances on anaerobic biofilms supported by polyurethane foam matrices. Environ Eng Sci 20, 249–255.CrossRefGoogle Scholar
Romaškevič, T., Budriene, S., Pielichowski, K. & Pielichowski, J. (2006). Application of polyurethanebased materials for immobilization of enzymes and cells: A review. Chemija 17, 74–89.Google Scholar
Stehr, G., Zoerner, B., Boettcher, B. & Koops, H.P. (1994). Exopolymers: An ecological characteristic of a floc attached ammonia oxidizing bacterium. Microb Ecol 30, 115–126.Google Scholar
Stoodley, P., de Beer, D. & Lappin-Scott, H.M. (1997). Influence of electric fields and pH on biofilm structure as related to the bioelectric. Antimicrob Agents Ch 41, 1876–1879.CrossRefGoogle Scholar
Stoodley, P., de Beer, D. & Lewandowski, Z. (1994). Liquid flow in biofilm systems. Appl Environ Microb 60, 2711–2716.CrossRefGoogle ScholarPubMed
Surman, S.B., Walker, J.T., Goddard, D.T., Morton, L.H.G., Keevil, C.W., Weaver, W., Skinner, A., Hanson, K., Caldwell, D. & Kurtz, J. (1996). Comparison of microscope techniques for the examination of biofilms. J Microbiol Meth 25, 57–70.CrossRefGoogle Scholar
Sutherland, I.W. (2001). The biofilm matrix—An immobilized but dynamic microbial environment. Trends Microbiol 9, 222–226.CrossRefGoogle ScholarPubMed
Weber, S.D., Ludwig, W., Schleifer, K-H. & Fried, J. (2007). Microbial composition and structure of aerobic granular sewage biofilms. Appl Environ Microb 73, 6233–6240.CrossRefGoogle ScholarPubMed
Woznica, A., Nowak, A., Beimfohr, C., Karczewski, J. & Bernas, T. (2010). Monitoring structure and activity of nitrifying bacterial biofilm in an automatic biodetector of water toxicity. Chemosphere 78, 1121–1128.CrossRefGoogle Scholar
Wuchter, C., Abbas, B., Coolen, M.J.L., Herfort, L., van Bleijswijk, J. & Timmers, P. (2006). Archaeal nitrification in the ocean. P Natl Acad Sci 103, 12317–12322.CrossRefGoogle ScholarPubMed
Xavier, J., Dekreuk, M., Picioreanu, C. & Vanloosdrecht, M.M. (2007). Multi-scale individual-based model of microbial and bioconversion dynamics in aerobic granular sludge. Environ Sci Technol 41, 6410–6417.CrossRefGoogle ScholarPubMed
Xi, C., Marks, D., Schlachter, S., Luo, W. & Boppart, S.A. (2006). High-resolution three-dimensional imaging of biofilm development using optical coherence tomography. J Biomed Opt 11, 1–6.CrossRefGoogle ScholarPubMed

Woznica Supplementary Material

Movie

Download Woznica Supplementary Material(Video)
Video 6.5 MB

Woznica Supplementary Material

Movie

Download Woznica Supplementary Material(Video)
Video 6.9 MB
Supplementary material: PDF

Woznica Supplementary Material

Figure.pdf

Download Woznica Supplementary Material(PDF)
PDF 378.8 KB