Skip to main content
SpringerLink
Log in

Presence of Acyl-Homoserine Lactone in Subtidal Biofilm and the Implication in Larval Behavioral Response in the Polychaete Hydroides elegans

  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Quorum sensing (QS) signals have been considered to play important roles in biofilm development and in the attractiveness of biofilms to higher organisms in marine ecosystem. In this study, bacterial QS signalsacylated homoserine lactone derivatives (AHLs) were detected in 2-, 4-, and 6-day-old subtidal biofilms by using AHLs reporter strains. N-dodecanoyl-homoserine lactone (C12-HSL) was identified in 6-day-old biofilm at a concentration of 9.04 μg cm−minus;2 (3.36 mmol l−minus;1). To investigate the possible role of AHLs in the consequent eventlarval settlement of the polychaete Hydroides elegans onto subtidal biofilmsseven biofilm-derived bacteria that effectively induced larval settlement of H. elegans, were screened for AHL production. One of them, the Vibrio sp. UST950701-007, produced N-hexanoyl-homoserine lactone (C6-HSL). Larval settlement bioassay showed that C6-HSL, C12-HSL, and 3-oxo-octanoyl-homoserine lactone (3-oxo-C8-HLS) at certain concentrations induced some initial larval settlement behaviors such as reducing swimming speed, crawling on the bottom. However, these AHLs did not effectively induce larval settlement in comparison to the effective settlement inducer 3-isobutyl-1-methylxanthine. The possible chemokinetic mechanism and indirect effects of AHLs on larval settlement are suggested.

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

Similar content being viewed by others

References

  1. Burmølle, M, Hansen, LH, Sørensen, SJ (2005) Use of a whole-cell biosensor and flow cytometry to detect AHL production by an indigenous soil community during decomposition of litter. Microb Ecol 50: 221–229

    Article  PubMed  CAS  Google Scholar 

  2. Cataldi, TRI, Bianco, G, Frommberger, M, Schmitt-Kopplin, Ph (2004) Direct analysis of selected N-acyl-l-homoserine lactones by gas chromatography/mass spectrometry. Rapid Commun Mass Spectrom 18: 1341–1344

    Article  PubMed  CAS  Google Scholar 

  3. Chhabra, SR, Philipp, B, Eberl, L, Givskov, M, Williams, P, Camara, M (2005) Extracellular communication in bacteria. Top Curr Chem 240: 279–315

    CAS  Google Scholar 

  4. Cooksey, KE, Wigglesworth-Cooksey, B (1995) Adhesion of bacteria and diatoms to surfaces in the sea—a review. Aquat Microb Ecol 9: 87–96

    Google Scholar 

  5. Costerton, JW, Lewandowski, Z, Caldwell, DE, Korber, DR, Lappin-Scott, HM (1995) Microbial biofilms. Annu Rev Microbiol 49: 711–745

    Article  PubMed  CAS  Google Scholar 

  6. Davies, DG, Parsek, MR, Pearson, JP, Iglewski, BH, Costerton, JW, Greenberg, EP (1998) The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science 280: 295–298

    Article  PubMed  CAS  Google Scholar 

  7. Dong, YH, Zhang, LH (2005) Quorum sensing and quorum-quenching enzymes. J Microbiol 43: 101–109

    PubMed  CAS  Google Scholar 

  8. Donlan, RM (2002) Biofilms: microbial life on surfaces. Emerg Infect Dis 8: 881–890

    PubMed  Google Scholar 

  9. Gram, L, Grossart, HP, Schlingloff, A, Kiorboe, T (2002) Possible quorum sensing in marine snow bacteria: production of acylated homoserine lactones by Roseobacter strains isolated from marine snow. Appl Environ Microbiol 68: 4111–4116

    Article  PubMed  CAS  Google Scholar 

  10. Greenberg, EP (2000) Acyl-homoserine lactone quorum sensing in bacteria. J Microbiol 38: 117–121

    CAS  Google Scholar 

  11. Harder, T, Lau, SCK, Dahms, HU, Qian, PY (2002) Isolation of bacterial metabolites as natural inducers for larval settlement in the marine polychaete Hydroides elegans (Haswell). J Chem Ecol 28: 2029–2043

    Article  PubMed  CAS  Google Scholar 

  12. Hassett, DJ, Ma, JF, Elkins, JG, McDermott, TR, Ochsner, UA, West, SE, Huang, CT, Fredericks, J, Burnett, S, Stewart, PS, McFeters, G, Passador, L, Iglewski, BH (1999) Quorum sensing in Pseudomonas aeruginosa controls expression of catalase and superoxide dismutase genes and mediates biofilm susceptibility to hydrogen peroxide. Mol Microbiol 34: 1082–1093

    Article  PubMed  CAS  Google Scholar 

  13. Huang, SY, Hadfield, MG (2003) Composition and density of bacterial biofilms determine larval settlement of the polychaete Hydroides elegans. Mar Ecol Prog Ser 260: 161–172

    CAS  Google Scholar 

  14. Jin, T, Qian, PY (2005) Amino acid exposure modulates the bioactivity of biofilms for larval settlement of Hydroides elegans by altering bacterial community components. Mar Ecol Prog Ser 297: 169–179

    CAS  Google Scholar 

  15. Joint, I, Tait, K, Callow, ME, Callow, JA, Milton, D, Williams, P, Camara, M (2002) Cell-to-cell communication across the prokaryote-eukaryote boundary. Science 298: 1207

    Article  PubMed  Google Scholar 

  16. Lau, SCK, Qian, PY (2001) Larval settlement in the serpulid polychaete Hydroides elegans in response to bacterial films: an investigation of the nature of putative larval settlement cue. Mar Biol 138: 321–328

    Article  Google Scholar 

  17. Lau, SCK, Mak, KKW, Chen, F, Qian, PY (2002) Bioactivity of bacterial strains isolated from marine biofilms in Hong Kong waters for the induction of larval settlement in the marine polychaete Hydroides elegans. Mar Ecol Prog Ser 226: 301–310

    Google Scholar 

  18. Lau, SCK, Harder, T, Qian, PY (2003) Induction of larval settlement in the serpulid polychaete Hydroides elegans (Haswell): role of bacterial extracellular polymers. Biofouling 19: 197–204

    Article  PubMed  CAS  Google Scholar 

  19. Lau, SCK, Thiyagarajan, V, Cheung, SCK, Qian, PY (2005) Roles of bacterial community composition in biofilms as a mediator for larval settlement of three marine invertebrates. Aquat Microb Ecol 38: 41–51

    Google Scholar 

  20. Lee, OO, Qian, PY (2003) Chemical control of bacterial epibiosis and larval settlement of Hydroides elegans in the red sponge Mycale adherens. Biofouling 19: 171–180

    Article  PubMed  CAS  Google Scholar 

  21. McClean, KH, Winson, MK, Fish, L, Taylor, A, Chhabra, SR, Camara, M, Daykin, M, Lamb, JH, Swift, S, Bycroft, BW, Stewart, GS, Williams, P (1997) Quorum sensing in Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones. Microbiology 143: 3703–3711

    Article  PubMed  CAS  Google Scholar 

  22. McLean, RJC, Whiteley, M, Stickler, DJ, Fuqua, WC (1997) Evidence of autoinducer activity in naturally occurring biofilms. FEMS Microbiol Lett 154: 259–263

    Article  PubMed  CAS  Google Scholar 

  23. McLean, RJC, Pierson, LS, Fuqua, C (2004) A simple screening protocol for the identification of quorum signal antagonists. J Microbiol Methods 58: 351–360

    Article  PubMed  CAS  Google Scholar 

  24. Miller, MB, Bassler, BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55: 165–199

    Article  PubMed  CAS  Google Scholar 

  25. Parsek, MR, Greenberg, EP (2005) Sociomicrobiology: the connections between quorum sensing and biofilms. Trends Microbiol 13: 27–33

    Article  PubMed  CAS  Google Scholar 

  26. Pasmore, M, Costerton, JW (2003) Biofilms, bacterial signaling, and their ties to marine biology. J Ind Microbiol Biotech 30: 407–413

    Article  CAS  Google Scholar 

  27. Pechenik, JA, Qian, PY (1998) Onset and maintenance of metamorphic competence in the marine polychaete Hydroides elegans Haswell in response to three chemical cues. J Exp Mar Biol Ecol 226: 51–74

    Article  Google Scholar 

  28. Qian, PY (1999) Larval settlement of polychaetes. Hydrobiologia 402: 239–253

    Article  CAS  Google Scholar 

  29. Quinn, GP, Keough, MJ (2002) Experimental Design and Data Analysis for Biologists. Cambridge University Press, Cambridge, UK, p 537

    Google Scholar 

  30. Ravn, L, Christensen, AB, Molin, S, Givskov, M, Gram, L (2001) Methods for detecting acylated homoserine lactones produced by Gram-negative bacteria and their application in studies of AHL-production kinetics. J Microbiol Methods 44: 239–251

    Article  PubMed  CAS  Google Scholar 

  31. Ruby, EG, Lee, KH (1998) The Vibrio fischeri euprymna scolopes light organ association: current ecological paradigms. Appl Environ Microbiol 64: 805–812

    PubMed  CAS  Google Scholar 

  32. Stoodley, P, Sauer, K, Davies, DG, Costerton, JW (2002) Biofilms as complex differentiated communities. Annu Rev Microbiol 56: 187–209

    Article  PubMed  CAS  Google Scholar 

  33. Szewzyk, U, Holmstrom, C, Wrangstadh, M, Samuelsson, MO, Maki, JS, Kjelleberg, S (1991) Relevance of the exopolysaccharide of marine Pseudomonas sp. strain S9 for the attachment of Ciona intestinalis larvae. Mar Ecol Prog Ser 75: 259–265

    Google Scholar 

  34. Tait, K, Joint, I, Daykin, M, Milton, DL, Williams, P, Camara, M (2005) Disruption of quorum sensing in seawater abolishes attraction of zoospores of the green alga Ulva to bacterial biofilms. Environ Microbiol 7: 229–240

    Article  PubMed  CAS  Google Scholar 

  35. Taylor, MW, Schupp, PJ, Baillie, HJ, Charlton, TS, de Nys, R, Kjelleberg, S, Steinberg, PD (2004) Evidence for acyl homoserine lactone signal production in bacteria associated with marine sponges. Appl Environ Microbiol 70: 4387–4389

    Article  PubMed  CAS  Google Scholar 

  36. Unabia, C, Hadfield, MG (1999) The role of bacteria in larval settlement and metamorphosis of the polychaete Hydroides elegans. Mar Biol 133: 55–64

    Article  Google Scholar 

  37. Wagner-Dobler, I, Thiel, V, Eberl, L, Allgaier, M, Bodor, A, Meyer, S, Ebner, S, Hennig, A, Pukall, R, Schulz, S (2005) Discovery of complex mixtures of novel long-chain quorum sensing signals in free-living and host-associated marine alphaproteobacteria. ChemBioChem 6: 2195–2206

    Article  PubMed  CAS  Google Scholar 

  38. Wheeler, GL, Tait, K, Taylor, A, Brownlee, C, Joint, I (2006) Acyl-homoserine lactones modulate the settlement rate of zoospores of the marine alga Ulva intestinalis via a novel chemokinetic mechanism. Plant Cell Environ 608–618

  39. Whitchurchm, CB, Tolker-Neilsen, T, Ragas, PC, Mattick, JS (2002) Extracellular DNA required for bacterial biofilm formation. Science 295: 1487

    Article  Google Scholar 

  40. Whitehead, NA, Barnard, AML, Slater, H, Simpson, NJL, Salmond, GPC (2001) Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 25: 365–404

    Article  PubMed  CAS  Google Scholar 

  41. Wieczorek, SK, Todd, CD (1998) Inhibition and facilitation of settlement of epifaunal marine invertebrate larvae by microbial biofilm cues. Biofouling 12: 81–118

    Article  Google Scholar 

  42. Winzer, K, Falconer, C, Garber, NC, Diggle, SP, Camara, M, William, P (2000) The Pseudomonas aeruginosa lectins PA-IL and PA-IIL are controlled by quorum sensing and by RpoSJ. J Bacteriol 182: 6401–6411

    Article  PubMed  CAS  Google Scholar 

  43. Zhang, LH, Dong, YH (2004) Quorum sensing and signal interference: diverse implications. Mol Microbiol 53: 1563–1571

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgment

The authors thank Professor Robert McLean (Department of Biology, Texas State University) for his kind gift of the AHLs reporter strains. We also thank Dr. On On Lee, Dr. Vengatesen Thiyagarajan, Dr. Hans-U. Dahms, Dr. Xiancui Li and Prof. Jan Pechenik for their valuable comments on this manuscript, and Mr. Oi Shing Hung for his assistance in larval bioassay. This study was supported by an RGC grants (CA04/05.Sc01, HKUST6402/05M) and a Croucher Foundation Research grant (CF-CAS03/04.Sc01) to Pei-Yuan Qian.

Author information

Authors and Affiliations

  1. Coastal Marine Laboratory/Department of Biology, Hong Kong University of Science and Technology, Clear Water Bay, Kowloon, Hong Kong, China

    Yi-Li Huang, Sergey Dobretsov, Jang-Seu Ki, Lai-Hung Yang & Pei-Yuan Qian

Authors
  1. Yi-Li Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sergey Dobretsov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jang-Seu Ki
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lai-Hung Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Pei-Yuan Qian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Pei-Yuan Qian.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Huang, YL., Dobretsov, S., Ki, JS. et al. Presence of Acyl-Homoserine Lactone in Subtidal Biofilm and the Implication in Larval Behavioral Response in the Polychaete Hydroides elegans . Microb Ecol 54, 384–392 (2007). https://doi.org/10.1007/s00248-007-9210-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-007-9210-9

Keywords

Search

Navigation