Skip to main content
SpringerLink
Log in

Bacterial Community Structure of Biofilms on Artificial Surfaces in an Estuary

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

This study examined bacterial community structure of biofilms on stainless steel and polycarbonate in seawater from the Delaware Bay. Free-living bacteria in the surrounding seawater were compared to the attached bacteria during the first few weeks of biofilm growth. Surfaces exposed to seawater were analyzed by using 16S rDNA libraries, fluorescence in situ hybridization (FISH), and denaturing gradient gel electrophoresis (DGGE). Community structure of the free-living bacterial community was different from that of the attached bacteria according to FISH and DGGE. In particular, alpha-proteobacteria dominated the attached communities. Libraries of 16S rRNA genes revealed that representatives of the Rhodobacterales clade were the most abundant members of biofilm communities. Changes in community structure during biofilm growth were also examined by DGGE analysis. We hypothesized that bacterial communities on dissimilar surfaces would initially differ and become more similar over time. In contrast, the compositions of stainless steel and polycarbonate biofilms were initially the same, but differed after about 1 week of biofilm growth. These data suggest that the relationship between surface properties and biofilm community structure changes as biofilms grow on surfaces such as stainless steel and polycarbonate in estuarine water.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6

Similar content being viewed by others

References

  1. Amann, RI, Krumholz, L, Stahl, DA (1990) Fluorescent oligonucleotide probing of whole cells for determinative, phylogenetic, and environmental studies in microbiology. J Bacteriol 172: 762–770

    PubMed  CAS  Google Scholar 

  2. Araya, R, Tani, K, Takagi, T, Yamaguchi, N, Nasu, M (2003) Bacterial activity and community composition in stream water and biofilm from an urban river determined by fluorescent in situ hybridization and DGGE analysis. FEMS Microbiol Ecol 43: 111–119

    Article  CAS  PubMed  Google Scholar 

  3. Beech, IB, Gaylarde, CC (1999) Recent advances in the study of biocorrosion—an overview. Rev Microbiol 30: 177–190

    Article  CAS  Google Scholar 

  4. Behrens, S, Ruhland, C, Inacio, J, Huber, H, Fonseca, A, Spencer-Martins, I, Fuchs, BM, Amann, R (2003) In situ accessibility of small-subunit rRNA of members of the domains Bacteria, Archaea, and Eucarya to Cy3-labeled oligonucleotide probes. Appl Environ Microbiol 69: 1748–1758

    Article  PubMed  CAS  Google Scholar 

  5. Bhosle, NB, Garg, A, Fernandes, L, Citon, P (2005) Dynamics of amino acids in the conditioning film developed on glass panels immersed in the surface seawaters of Dona Paula Bay. Biofouling 21: 99–107

    Article  PubMed  CAS  Google Scholar 

  6. Bidle, KD, Fletcher, M (1995) Comparison of free-living and particle-associated bacterial communities in the Chesapeake bay by stable low-molecular-weight RNA analysis. Appl Environ Microbiol 61: 944–952

    PubMed  CAS  Google Scholar 

  7. Bruhn, JB, Nielsen, KF, Hjelm, M, Hansen, M, Bresciani, J, Schulz, S, Gram, L (2005) Ecology, inhibitory activity, and morphogenesis of a marine antagonistic bacterium belonging to the Roseobacter clade. Appl Environ Microbiol 71: 7263–7270

    Article  PubMed  CAS  Google Scholar 

  8. Brummer, IHM, Fehr, W, Wagner-Dobler, I (2000) Biofilm community structure in polluted rivers: abundance of dominant phylogenetic groups over a complete annual cycle. Appl Environ Microbiol 66: 3078–3082

    Article  PubMed  CAS  Google Scholar 

  9. Castle, D, Kirchman, DL (2004) Composition of estuarine bacterial communities assessed by denaturing gradient gel electrophoresis and fluorescence in situ hybridization. Limnol Oceanogr Methods 2: 303–314

    Google Scholar 

  10. Compere, C, Bellon-Fontaine, MN, Bertrand, P, Costa, D, Marcus, P, Poleunis, C, Pradier, CM, Rondot, B, Walls, MG (2001) Kinetics of conditioning layer formation on stainless steel immersed in seawater. Biofouling 17: 129–145

    Article  Google Scholar 

  11. Cottrell, MT, Kirchman, DL (2000) Community composition of marine bacterioplankton determined by 16S rRNA gene clone libraries and fluorescence in situ hybridization. Appl Environ Microbiol 66: 5116–5122

    Article  PubMed  CAS  Google Scholar 

  12. Cottrell, MT, Kirchman, DL (2003) Contribution of major bacterial groups to bacterial biomass production (thymidine and leucine incorporation) in the Delaware estuary. Limnol Oceanogr 48: 168–178

    Article  Google Scholar 

  13. Cottrell, MT, Kirchman, DL (2000) Natural assemblages of marine proteobacteria and members of the Cytophaga–Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Appl Environ Microbiol 66: 1692–1697

    Article  PubMed  CAS  Google Scholar 

  14. Crump, BC, Armbrust, EV, Baross, JA (1999) Phylogenetic analysis of particle-attached and free-living bacterial communities in the Columbia River, its estuary, and the adjacent coastal ocean. Appl Environ Microbiol 65: 3192–3204

    PubMed  CAS  Google Scholar 

  15. D’Souza, F, Garg, A, Bhosle, NB (2005) Seasonal variation in the chemical composition and carbohydrate signature compounds of biofilm. Aquat Microb Ecol 41: 199–207

    Google Scholar 

  16. Dang, HY, Lovell, CR (2000) Bacterial primary colonization and early succession on surfaces in marine waters as determined by amplified rRNA gene restriction analysis and sequence analysis of 16S rRNA genes. Appl Environ Microbiol 66: 467–475

    Article  PubMed  CAS  Google Scholar 

  17. Dang, HY, Lovell, CR (2002) Numerical dominance and phylotype diversity of marine Rhodobacter species during early colonization of submerged surfaces in coastal marine waters as determined by 16S ribosomal DNA sequence analysis and fluorescence in situ hybridization. Appl Environ Microbiol 68: 496–504

    Article  PubMed  CAS  Google Scholar 

  18. Dang, HY, Lovell, CR (2002) Seasonal dynamics of particle-associated and free-living marine Proteobacteria in a salt marsh tidal creek as determined using fluorescence in situ hybridization. Environ Microbiol 4: 287–295

    Article  PubMed  CAS  Google Scholar 

  19. DeLong, EF, Franks, DG, Alldredge, AL (1993) Phylogenetic diversity of aggregate-attached vs free-living marine bacterial assemblages. Limnol Oceanogr 38: 924–934

    Article  Google Scholar 

  20. Francis, CA, Co, EM, Tebo, BM (2001) Enzymatic manganese(II) oxidation by a marine alpha-proteobacterium. Appl Environ Microbiol 67: 4024–4029

    Article  PubMed  CAS  Google Scholar 

  21. Fuchs, BM, Wallner, G, Beisker, W, Schwippl, I, Ludwig, W, Amann, R (1998) Flow cytometric analysis of the in situ accessibility of Escherichia coli 16S rRNA for fluorescently labeled oligonucleotide probes. Appl Environ Microbiol 64: 4973–4982

    PubMed  CAS  Google Scholar 

  22. Giovannoni, SJ, Britschgi, TB, Moyer, CL, Field, KG (1990) Genetic diversity in Sargasso Sea bacterioplankton. Nature 345: 60–63

    Article  PubMed  CAS  Google Scholar 

  23. Glöckner, FO, Fuchs, BM, Amann, R (1999) Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl Environ Microbiol 65: 3721–3726

    PubMed  Google Scholar 

  24. Jones, PR (2005) Community Structure of Bacterial Biofilms on Stainless Steel in the Delaware Bay. M.S. University of Delaware, Lewes

    Google Scholar 

  25. Karner, M, Fuhrman, JA (1997) Determination of active marine bacterioplankton: a comparison of universal 16S rRNA probes, autoradiography, and nucleoid staining. Appl Environ Microbiol 63: 1208–1213

    PubMed  CAS  Google Scholar 

  26. Keil, RG, Kirchman, DL (1999) Utilization of dissolved protein and amino acids in the northern Sargasso Sea. Aquat Microb Ecol 18: 293–300

    Google Scholar 

  27. Lane, DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt, E, Goodfellow, M (Eds.), Nucleic Acid Techniques in Bacterial Systematics. Wiley, New York, pp 115–175

    Google Scholar 

  28. Ling, SC, Alldredge, AL (2003) Does the marine copepod Calanus pacificus consume transparent exopolymer particles (TEP)?J Plankton Res 25: 507–515

    Article  CAS  Google Scholar 

  29. Ludwig, W, Strunk, O, Westram, R, Richter, L, Meier, H, Yadhukumar, Buchner, A, Lai, T, Steppi, S, Jobb, G, Forster, W, Brettske, I, Gerber, S, Ginhart, AW, Gross, O, Grumann, S, Hermann, S, Jost, R, Konig, A, Liss, T, Lussmann, R, May, M, Nonhoff, B, Reichel, B, Strehlow, R, Stamatakis, A, Stuckmann, N, Vilbig, A, Lenke, M, Ludwig, T, Bode, A, Schleifer, KH (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363–1371

    Article  PubMed  CAS  Google Scholar 

  30. Manz, W, Amann, R, Ludwig, W, Vancanneyt, M, Schleifer, KH (1996) Application of a suite of 16S rRNA-specific oligonucleotide probes designed to investigate bacteria of the phylum Cytophaga–Flavobacter–Bacteroides in the natural environment. Microbiology UK 142: 1097–1106

    Article  CAS  Google Scholar 

  31. Manz, W, Amann, R, Ludwig, W, Wagner, M, Schleifer, KH (1992) Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria—problems and solutions. Syst Appl Microbiol 15: 593–600

    Google Scholar 

  32. McLean, RJC, Barnes, MB, Windham, MK, Merchant, M, Forstner, MRJ, Fuqua, C (2005) Cell–cell influences on bacterial community development in aquatic biofilms. Appl Environ Microbiol 71: 8987–8990

    Article  PubMed  CAS  Google Scholar 

  33. Mueller, RF (1996) Bacterial transport and colonization in low nutrient environments. Water Res 30: 2681–2690

    Article  CAS  Google Scholar 

  34. Muyzer, G, Dewaal, EC, Uitterlinden, AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S ribosomal-RNA. Appl Environ Microbiol 59: 695–700

    PubMed  CAS  Google Scholar 

  35. O’Sullivan, LA, Weightman, AJ, Fry, JC (2002) New degenerate Cytophaga–Flexibacter–Bacteroides-specific 16S ribosomal DNA-targeted oligonucleotide probes reveal high bacterial diversity in River Taff epilithon. Appl Environ Microbiol 68: 201–210

    Article  PubMed  CAS  Google Scholar 

  36. Rath, J, Wu, KY, Herndl, GJ, DeLong, EF (1998) High phylogenetic diversity in a marine-snow-associated bacterial assemblage. Aquat Microb Ecol 14: 261–269

    Google Scholar 

  37. Reichenbach, H (1991) The order Cytophagales. In: Balows, A (Ed.), The Prokaryotes. Springer-Verlag, New York, pp 3631–3675

    Google Scholar 

  38. Sharp, JH, Culberson, CH, Church, TM (1982) The chemistry of the Delaware estuary. General considerations. Limnol Oceanogr 27: 1015–1028

    Article  CAS  Google Scholar 

  39. Siering, PL, Ghiorse, WC (1997) Development and application of 16S rRNA-targeted probes for detection of iron- and manganese-oxidizing sheathed bacteria in environmental samples. Appl Environ Microbiol 63: 644–651

    PubMed  CAS  Google Scholar 

  40. Simon, M, Grossart, HP, Schweitzer, B, Ploug, H (2002) Microbial ecology of organic aggregates in aquatic ecosystems. Aquat Microb Ecol 28: 175–211

    Google Scholar 

  41. Sreekumari, KR, Sato, Y, Kikuchi, Y (2005) Antibacterial metals—a viable solution for bacterial attachment and microbiologically influenced corrosion. Mater Trans 46: 1636–1645

    Article  CAS  Google Scholar 

  42. Suzuki, MT, Giovannoni, SJ (1996) Bias caused by template annealing in the amplification of mixtures of 16S rRNA genes by PCR. Appl Environ Microbiol 62: 625–630

    PubMed  CAS  Google Scholar 

  43. Videla, HA, Characklis, WG (1992) Biofouling and microbially influenced corrosion. Int Biodeter Biodegr 29: 195–212

    Article  CAS  Google Scholar 

  44. Videla, HA, Herrera, LK (2005) Microbiologically influenced corrosion: looking to the future. Int Microbiol 8: 169–180

    PubMed  CAS  Google Scholar 

  45. von Wintzingerode, F, Gobel, UB, Stackebrandt, E (1997) Determination of microbial diversity in environmental samples: pitfalls of PCR-based rRNA analysis. FEMS Microbiol Rev 21: 213–229

    Article  Google Scholar 

  46. Weller, R, Glöckner, FO, Amann, R (2000) 16S rRNA-targeted oligonucleotide probes for the in situ detection of members of the phylum Cytophaga–Flavobacterium–Bacteroides. Syst Appl Microbiol 23: 107–114

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the U.S. Office of Naval Research (N00014-05-1-0201) and the U.S. Department of Energy BIOMP (DF-FG02-97 ER 62479). We thank Liying Yu for her invaluable guidance and assistance. The efforts of Olivia Hauser were instrumental during the initial phases of the molecular work and Xia Bai's help with the seawater exposure experiments was greatly appreciated.

Author information

Authors and Affiliations

  1. College of Marine and Earth Studies, University of Delaware, 700 Pilottown Road, Lewes, DE, 19958, USA

    Paul R. Jones, Matthew T. Cottrell, David L. Kirchman & Stephen C. Dexter

Authors
  1. Paul R. Jones
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthew T. Cottrell
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David L. Kirchman
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stephen C. Dexter
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Matthew T. Cottrell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jones, P.R., Cottrell, M.T., Kirchman, D.L. et al. Bacterial Community Structure of Biofilms on Artificial Surfaces in an Estuary. Microb Ecol 53, 153–162 (2007). https://doi.org/10.1007/s00248-006-9154-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-006-9154-5

Keywords

Search

Navigation