Inhibition of the reattachment of young adult zebra mussels by single-species biofilms and associated exopolymers

Journal of Applied Microbiology

Volumn 97, Issue 6, 2004, Pages 1236-1246

  Kavouras, J H ^a   Maki, J S ^a  

^a Marquette University   (United States)

Author keywords

Biofilms; Extracellular products; Substratum; Zebra mussels

Indexed keywords

ANALYSIS OF VARIANCE (ANOVA); BACTERIA; GLASS; MOLLUSCS; POLYSTYRENES;

BACTERIAL FILMS; BYSSAL THREADS; EXOPOLYMERS; EXTRACELLULAR; EXTRACELLULAR PRODUCT; GLASS SURFACES; SINGLE SPECIES; SUBSTRATUM; YOUNG ADULTS; ZEBRA MUSSELS;

BIOFILMS;

GLASS; POLYMER; POLYSTYRENE;

BIOFILM; MOLLUSC; SUBSTRATE;

ARTICLE; BACTERIAL STRAIN; BIOFILM; CONTROLLED STUDY; DREISSENA; MUSSEL; NONHUMAN; PLANKTON;

BACTERIA (MICROORGANISMS); DREISSENA POLYMORPHA; MOLLUSCA;

EID: 9644270362     PISSN: 13645072     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2672.2004.02410.x     Document Type: Article

References (52)

1. Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Research 25, 3389-3402.
2. Ashwell, G. (1966) New colorimetric methods of sugar analysis. Methods in Enzymology 8, 85-95.
3. Baier, R.E., Shafrin, E.G. and Zisman, W.A. (1968) Adhesion: mechanisms that assist or impede it. Science 162, 1360-1368.
4. Beech, I., Hanjagsit, L., Kalaji, M., Neal, A.L. and Zinkevich, V. (1999) Chemical and structural characterization of exopolymers produced by Pseudomonas sp. NCIMB 2021 in continuous culture. Microbiology 145, 1491-1497.
5. Bradford, M.M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248-254.
6. Burton, N.F., Day, M.J. and Bull, A.T. (1982) Distribution of plasmids in clean and polluted sites in a South Wales river. Applied and Environmental Microbiology 44, 1026-1029.
7. Cavanaugh, G.M. (1975) Formulae and Methods VI of the Marine Biological Laboratory Chemical Room. 84 pp. Woods Hole, MA: Marine Biological Laboratory.
8. Crisp, D.J. (1984) Overview of research on marine invertebrate larvae, 1940-1980. In Marine Biodeterioration: An Interdisciplinary Study ed. Costlow, J.D. and Tipper, R.C. pp. 103-126. Annapolis, MD: Naval Institute Press.
9. Davies, D.G., Chakrabarty, A.M. and Geesey, G.G. (1993) Exopolysaccharide production in biofilms: substratum activation of alginate gene expression by Pseudomonas aeruginosa. Applied and Environmental Microbiology 59, 1181-1186.
10. Eckroat, L.E., Masteller, E.G., Shaffer, J.C. and Steele, L.M. (1993) The byssus of the zebra mussel (Dreissena polymorpha): morphology, byssal thread formation, and detachment. In Zebra Mussels: Biology, Impacts, and Control ed. Nalepa, T.F. and Schloesser, D.W. pp. 39-53. Boca Raton: Lewis Publishers.
11. Fitt, W.K., Labare, M.P., Fuqua, C., Walch, M., Coon, S.L., Bonar, D.B., Colwell, R.R. and Weiner, R.M. (1989) Factors influencing bacterial production of inducers of settlement behavior of larvae of the oyster Crassostrea gigas. Microbial Ecology 17, 287-298.
12. Gerhart, D.J., Rittschof, D., Hooper, I.R., Eiseman, K., Meyer, A.E., Baier, R.E. and Young, C. (1992) Rapid and inexpensive quantification of the combined polar components of surface wettability: application to biofouling. Biofouling 5, 251-259.
13. Gherna, R. L. (1994) Culture preservation. In Methods for General and Molecular Bacteriology ed. Gerhardt, P., Murray, R.G.E., Wood, W.A. and Krieg, N.R. pp. 278-292. Washington, DC: American Society for Microbiology.
14. Hebert, P.D., Muncaster, B.W. and Mackie, G.L. (1989) Ecological and genetic studies on Dreissena polymorpha (Pallas): a new mollusc in the Great Lakes. Canadian Journal of Fisheries and Aquatic Sciences 46, 1587-1591.
15. Holmström, C. and Kjelleberg, S. (1999) Factors influencing the settlement of macrofoulers. In Recent Advances in Marine Biotechnology Vol. 3, Biofilms, Bioadhesion, Corrosion, and Biofouling ed. Fingerman, M., Nagabhushanam, R. and Thompson, M.-F. pp. 173-201. Enfield, NH: Science Publishers, Inc.
16. Holmström, C., Rittschof, D. and Kjelleberg, S. (1992) Inhibition of settlement by larvae of Balanus amphitrite and Ciona intestinalis by a surface-colonizing marine bacterium. Applied and Environmental Microbiology 58, 2111-2115.
17. Hudson, M.C. and Curtiss, R. (1990) Regulation of expression of Streptococcus mutans genes important to virulence. Infection and Immunity 58, 464-470.
18. Kavouras, J.H. and Maki, J.S. (2003a) Effects of biofilms on zebra mussel postveliger attachment to artificial surfaces. Invertebrate Biology 122, 138-151.
19. Kavouras, J.H. and Maki, J.S. (2003b) The effects of natural biofilms on the reattachment of young adult zebra mussels to artificial substrata. Biofouling 19, 247-256.
20. Kobak, J. (2001) Light, gravity and conspecifics as cues to site selection and attachment behaviour of juvenile and adult Dreissena polymorpha Pallas, 1771. Journal of Molluscan Studies 67, 183-189.
21. Lane, D.J. (1991) 16S/23S rRNA sequencing. In Nucleic Acid Techniques in Bacterial Systematics ed. Stackebrandt, E. and Goodfellow, M. pp. 115-175. New York: John Wiley and Sons.
22. Lawrence, J.R., Korber, D.R., Hoyle, B.D., Costerton, J.W., and Caldwell, D.E. (1991) Optical sectioning of microbial biofilms. Journal of Bacteriology 173, 6558-6567.
23. Lewandowski, K. (1976) Unionidae as a substratum for Dreissena polymorpha Pall. Polish Archives of Hydrobiology 23, 409-420.
24. Maki, J.S. (1999) The influence of marine microbes on biofouling. In Recent Advances in Marine Biotechnology Vol. 3, Biofilms, Bioadhesion, Corrosion, and Biofouling ed. Fingerman, M., Nagabhushanam, R., and Thompson, M.-F. pp. 147-171. Enfield, NH: Science Publishers, Inc.
25. Maki, J.S., Rittschof, D., Samuelsson, M.-O., Szewzyk, U., Yule, A.B., Kjelleberg, S., Costlow, J.D. and Mitchell, R. (1990a) Effect of marine bacteria and their exopolymers on the attachment of barnacle cypris larvae. Bulletin of Marine Science 46, 499-511.
26. Maki, J.S., Little, B.J., Wagner, P. and Mitchell, R. (1990b) Biofilm formation on metal surfaces in Antarctic waters. Biofouling 2, 27-38.
27. Maki, J.S., Yule, A.B., Rittschof, D. and Mitchell, R. (1994) The effect of bacterial films on the temporary adhesion and permanent fixation of cypris larvae, Balanus amphitrite Darwin. Biofouling 8, 121-131.
28. Maki, J.S., Patel, G. and Mitchell, R. (1998) Experimental pathogenicity of Aeromonas spp. For the zebra mussel, Dreissena polymorpha. Current Microbiology 36, 19-23.
29. Maki, J.S., Ding, L., Stokes, J., Kavouras, J.H. and Rittschof, D. (2000) Substratum/bacterial interactions and larval attachment: films and exopolysaccharides of Halomonas marina (ATCC 25374) and their effect on barnacle cyprid larvae, Balanus amphitrite Darwin. Biofouling 16, 159-170.
30. Marsden, J.E. and Lansky, D.M. (2000) Substrate selection by settling zebra mussels, Dreissena polymorpha, relative to material, texture, orientation and sunlight. Canadian Journal of Zoology 78, 787-793.
31. Martel, A. (1993) Dispersal and recruitment of zebra mussel (Dreissena polymorpha) in a nearshore area in west-central Lake Erie: the significance of postmetamorphic drifting. Canadian Journal of Fisheries and Aquatic Sciences 50, 3-12.
32. McMahon, R.F. and Bogan, A.E. (2001) Mollusca: Bivalvia. In Ecology and Classification of North American Freshwater Invertebrates ed. Thorp, J.H. and Covich, A.P. pp. 331-429. New York: Academic Press.
33. Morton, B. (1997) The aquatic nuisance species problem: a global perspective and review. In Zebra Mussels and Aquatic Nuisance Species. ed. D'Itri, F.M. pp. 1-54. Chelsea, MI: Ann Arbor Press, Inc.
34. Neal, A.L., and Yule, A.B. (1994) The interaction between Elminius modestus Darwin cyprids and biofilms of Deleya marina NCMB1877. Journal of Experimental Marine Biology and Ecology 176, 127-139.
35. O'Connor, N.J. and Richardson, D.L. (1996) Effects of bacterial films on attachment of barnacle (Balanus improvisus Darwin) larvae: laboratory and field studies. Journal of Experimental Marine Biology and Ecology 206, 69-81.
36. O'Connor, N.J. and Richardson, D.L. (1998) Attachment of barnacle (Balanus amphitrite Darwin) larvae: responses to bacterial films and extracellular materials. Journal of Experimental Marine Biology and Ecology 226, 115-129.
37. Oldham, C. (1930) Locomotive habit of Dreissena polymorpha. Journal of Conchology 19, 25-26.
38. Pfennig, N. and Wagener, S. (1986) An improved method of preparing wet mounts for photomicrographs of microorganisms. Journal of Microbiological Methods 4, 303-306.
39. Platt, R.M., Geesey, G.G., Davis, J.D. and White, D.C. (1985) Isolation and partial chemical analysis of firmly bound exopolysaccharide from adherent cells of a freshwater sediment bacterium. Canadian Journal of Microbiology 31, 675-680.
40. Reasoner, D.J. and Geldreich, E.E. (1985) A new medium for the enumeration and subculture of bacteria from potable water. Applied and Environmental Microbiology 49, 1-7.
41. Ricciardi, A., Neves, R.J. and Rasmussen, J.B. (1998) Impending extinctions of North American freshwater mussels (Unionoida) following the zebra mussel (Dreissena polymorpha) invasion. Journal of Animal Ecology 67, 613-619.
42. Rittschof, D., Forward, R.B., Jr, Cannon, G., Welch, J.M., McClary, M., Jr, Holm, E.R., Clare, A.E., Conova, S. et al. (1998) Cues and context: larval responses to physical and chemical cues. Biofouling 12, 31-44.
43. Schloesser, D.W. and Nalepa, T.F. (1994) Dramatic decline of unionid bivalves in offshore waters of western Lake Erie after infestation by the zebra mussel, Dreissena polymorpha. Canadian Journal of Fisheries and Aquatic Sciences 51, 2234-2242.
44. Skoog, D.A. (1998) An introduction to ultraviolet/visible molecular absorption spectrometry. In Principles of Instrumental Analysis, 5th edn ed. Skoog, D.A., Holler, F.J. and Nieman, T.A. pp. 300-328. Chicago, IL: Harcourt Brace College Publishers.
45. Smibert, R.M. and Krieg, N.R. (1994) Phenotypic characterization. In Methods for General and Molecular Bacteriology ed. Gerhardt, P., Murray, R.G.E., Wood, W.A. and Krieg, N.R. pp. 649-650. Washington, DC: American Society for Microbiology.
46. Smit, H., bij de Vaate, A., Reeders, H.H., van Nes, E.H. and Noordhuis, R. (1993) Colonization, ecology, and positive aspects of zebra mussels (Dreissena polymorpha) in the Netherlands. In Zebra Mussels: Biology, Impacts, and Control ed. Nalepa, T.F. and Schloesser, D.W. pp. 55-77. Boca Raton: Lewis Publishers.
47. Sprung, M. (1993) The other life: an account of present knowledge of the larval phase of Dreissena polymorpha. In Zebra Mussels: Biology, Impacts, and Control ed. Nalepa, T.F. and Schloesser, D.W. pp. 39-53. Boca Raton: Lewis Publishers.
48. Toomey, M.B., McCabe, D. and Marsden, J.E. (2002) Factors affecting the movement of adult zebra mussels. Journal of the North American Benthological Society 21, 468-475.
49. Vandevivere, P. and Kirchman, D.L. (1993) Attachment stimulates exopolysaccharide synthesis by a bacterium. Applied and Environmental Microbiology 59, 3280-3286.
50. Wainman, B.C., Hincks, S.S., Kaushik, N.K, and Mackie, G.L. (1996) Biofilm and substrate preference in the dreissenid larvae of Lake Erie. Canadian Journal of Fisheries and Aquatic Sciences 53, 134-140.
51. Wieczorek, S.K., and Todd C. (1998) Inhibition and facilitation of settlement of epifaunal marine invertebrate larvae by microbial biofilm cues. Biofouling 12, 81-118.
52. Zar, J. H. (1999) Biostatistical Analysis. 663 pp. Upper Saddle River, NJ: Prentice-Hall, Inc.