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Larval metamorphosis of the mussel Mytilus galloprovincialis in response to Alteromonas sp. 1: evidence for two chemical cues?

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Abstract

Bacterial isolates from multi-species biofilms were identified by 16S rDNA gene sequences and investigated for their inductive effects as monospecific biofilms on larval metamorphosis of Mytilus galloprovincialis. Alteromonas sp. 1 biofilm was found to have inductive activity, which increased with increasing cell density. The cue(s) of Alteromonas sp. 1 biofilm responsible for inducing larval metamorphosis was further investigated. Treatment of the biofilm with formalin, ethanol, heat or ultraviolet irradiation resulted in a significant reduction in the inductive activity of Alteromonas sp. 1, and the crude extract of surface-bound products of the biofilm showed no activity. These results indicated that if the cue was a surface-bound chemical cue, it was unstable, or susceptible to the treatments or the extraction process. On the other hand, the inductive activity of treated biofilms had a linear regression to the cell survival of bacteria, indicating a metabolically active biofilm was a requirement for larval metamorphosis. Conditioned water of the biofilm did not induce larvae to metamorphose. However, larval crawling behavior in the conditioned water was the same as that in the biofilm prior to larval metamorphosis, and significantly different to larval behavior in seawater. This indicated that a potential or partial waterborne cue existed, but remained inactive when alone. A synergistic effect of the conditioned water with formalin-fixed Alteromonas sp. 1 biofilm resulted in a significant increase in larval metamorphosis. Heat treatment and fractionation of the conditioned water demonstrated that the waterborne cue was heat-stable and <3,000 Da in molecular weight. Platinum-coating, Lentil Lectin and Wheat Germ Agglutinin treatments of the formalin-fixed biofilm significantly reduced its synergistic effect with the conditioned water, suggesting that a surface-bound cue was present on the biofilm and that the cue might be associated with the bacterial exopolysaccharide or glycoprotein. Evidence presented here suggests that two chemical cues derived from bacteria act synergistically on larval metamorphosis of Mytilus galloprovincialis.

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References

  • Bao WY, Satuito CG, Yang JL, Kitamura H (2007) Larval settlement and metamorphosis of the mussel Mytilus galloprovincialis in response to biofilms. Mar Biol 150:565–574

    Article  Google Scholar 

  • Cáceres-Martínez J, Robledo JA, Figueras A (1994) Settlement and post-larvae behavior of Mytilus galloprovincialis: field and laboratory experiments. Mar Ecol Prog Ser 112:107–117

    Article  Google Scholar 

  • Dahms HU, Dobretsov S, Qian PY (2004) The effect of bacterial and diatom biofilms on the settlement of the bryozoan Bugula neritina. J Exp Mar Biol Ecol 313:191–209

    Article  Google Scholar 

  • Fitt WK, Coon SL, Walch M, Weiner RM, Colwell RR, Bonar DB (1990) Settlement behavior and metamorphosis of oyster larvae (Crassostrea gigas) in response to bacterial supernatants. Mar Biol 106:389–394

    Article  Google Scholar 

  • García-Lavandeira M, Silva A, Abad M, Pazos AJ, Sánchez JL, Pérez-Parallé ML (2005) Effects of GABA and epinephrine on the settlement and metamorphosis of the larvae of four species of bivalve molluscs. J Exp Mar Biol Ecol 316:149–156

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Huggett MJ, Williamson JE, de Nys R, Kjelleberg S, Steinberg PD (2006) Larval settlement of the common Australian sea urchin Heliocidaris erythrogramma in response to bacteria from the surface of coralline algae. Oecologia 149:604–619

    Article  Google Scholar 

  • Johnson CR, Sutton DC (1994) Bacteria on the surface of crustose coralline algae induce metamorphosis of the crown-of-thorns starfish Acanthaster planci. Mar Biol 120:305–310

    Article  Google Scholar 

  • Johnson CR, Muir DG, Reysenbach AL (1991) Characteristic bacteria associated with surfaces of coralline algae: a hypothesis for bacterial induction of marine invertebrate larvae. Mar Ecol Prog Ser 74:281–294

    Article  Google Scholar 

  • Khandeparker L, Anil AC, Raghukumar S (2003) Barnacle larval destination: piloting possibilities by bacteria and lectin interaction. J Exp Mar Biol Ecol 289:1–13

    Article  Google Scholar 

  • Kirchman D, Graham S, Reish D, Mitchell R (1982a) Bacteria induce settlement and metamorphosis of Janua (Dexiospira) brasiliensis Grube (Polychaeta: Spirorbidae). J Exp Mar Biol Ecol 56:153–163

    Article  Google Scholar 

  • Kirchman D, Graham S, Reish D, Mitchell R (1982b) Lectins may mediate in the settlement and metamorphosis of Janua (Dexiospira) brasiliensis Grube (Polychaeta: Spirorbidae). Mar Biol Lett 3:131–142

    CAS  Google Scholar 

  • Kogure K, Simidu U, Taga N (1979) A tentative direct microscopic method for counting living marine bacteria. Can J Microbiol 25:415–420

    Article  CAS  Google Scholar 

  • Kogure K, Simidu U, Taga N (1984) An improved direct viable count method for aquatic bacteria. Arch Hydrobiol 102:117–122

    Google Scholar 

  • 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 

  • Lau SCK, Harder T, Qian PY (2003a) Induction of larval settlement in the serpulid polychaete Hydroides elegans (Haswell): role of bacterial extracellular polymers. Biofouling 19(3):197–204

    Article  CAS  Google Scholar 

  • Lau SCK, Thiyagarajan V, Qian PY (2003b) The bioactivity of bacterial isolates in Hong Kong waters for the inhibition of barnacle (Balanus amphitrite Darwin) settlement. J Exp Mar Biol Ecol 282:43–60

    Article  Google Scholar 

  • Leitz T, Wagner T (1993) The marine bacterium Alteromonas espejiana induces metamorphosis of the hydroid Hydractinia echinata. Mar Biol 115:173–178

    Article  Google Scholar 

  • Maki JS, Mitchell R (1985) Involvement of lectins in the settlement and metamorphosis of marine invertebrate larvae. Bull Mar Sci 37:675–683

    Google Scholar 

  • Maki JS, Rittschof D, Schmidt AR, Snyder AG, Mitchell R (1989) Factors controlling attachment of bryozoan larvae: a comparison of bacterial films and unfilmed surfaces. Biol Bull 177:295–302

    Article  Google Scholar 

  • Negri AP, Webster NS, Hill RT, Heyward AJ (2001) Metamorphosis of broadcast spawning corals in response to bacteria isolated from crustose algae. Mar Ecol Prog Ser 223:121–131

    Article  Google Scholar 

  • Neumann R (1979) Bacterial induction of settlement and metamorphosis in the planula larvae of Cassiopea andromeda (Cnidaria: Scyphozoa, Rhizostomeae). Mar Ecol Prog Ser 1:21–28

    Article  Google Scholar 

  • Olivier F, Tremblay R, Bourget E, Rittschof D (2000) Barnacle settlement: field experiments on the influence of larval supply, tidal level, biofilm quality and age on Balanus amphitrite cyprids. Mar Ecol Prog Ser 199:185–204

    Article  Google Scholar 

  • Rahim SAKA, Li JY, Kitamura H (2004) Larval metamorphosis of the sea urchins, Pseudocentrotus depressus and Anthocidaris crassispina in response to microbial films. Mar Biol 144:71–78

    Article  Google Scholar 

  • Ramírez SC, Cáceres-Martínez J (1999) Settlement of the blue mussel Mytilus galloprovincialis Larmark on artificial substrates in Bahía de Todos Santos B.C., México. J Shellfish Res 18(1):33–39

    Google Scholar 

  • Rittschof D (1990) Peptide-mediated behaviors in marine organisms: evidence for a common theme. J Chem Ecol 16(1):261–272

    Article  CAS  Google Scholar 

  • Satuito CG, Natoyama K, Yamazaki M, Fusetani N (1995) Induction of attachment and metamorphosis of laboratory cultured mussel Mytilus edulis galloprovincialis larvae by biofilm. Fisheries Sci 61(2):223–227

    Article  CAS  Google Scholar 

  • Satuito CG, Natoyama K, Yamazaki M, Shimizu K, Fusetani N (1999) Induction of metamorphosis in the pediveliger larvae of the mussel Mytilus galloprovincialis by neuroactive compounds. Fisheries Sci 65(3):384–389

    Article  CAS  Google Scholar 

  • Satuito CG, Bao WY, Yang JL, Kitamura H (2005) Survival, growth, settlement and metamorphosis of refrigerated larvae of the mussel Mytilus galloprovincialis Lamarck and their use in settlement and antifouling bioassays. Biofouling 21(3/4):217–225

    Article  Google Scholar 

  • Steinberg PD, de Nys R, Kjelleberg S (2001) Chemical mediation of surface colonization. In: McClintock JB, Baker JB (eds) Marine chemical ecology. CRC Press, Boca Raton, pp 431–460

    Google Scholar 

  • Szewzyk U, Holmström 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

    Article  Google Scholar 

  • Unabia CRC, Hadfield MG (1999) Role of bacteria in larval settlement and metamorphosis of the polychaete Hydroides elegans. Mar Biol 133:55–64

    Article  Google Scholar 

  • Weiner RM, Walch M, Labare MP, Bonar DB, Colwell RR (1989) Effect of biofilms of the marine bacterium Alteromonas colwelliana (LST) on set of the oysters Crassostrea gigas (Thunberg, 1793) and C. virginica (Gmelin, 1791). J Shellfish Res 8(1):117–123

    Google Scholar 

  • Wieczorek SK, Clare AS, Todd CD (1995) Inhibitory and facilitatory effect of biofilms on settlement of Balanus amphitrite larvae. Mar Ecol Prog Ser 119:221–228

    Article  Google Scholar 

  • Zimmer-Faust RK, Tamburri MN (1994) Chemical identity and ecological implications of a waterborne, larval settlement cue. Limnol Oceanogr 39(5):1075–1087

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors are grateful to Dr. K. Kanai of Nagasaki University for guidance in the identification of the bacteria and the staff of the Nagasaki Prefectural Institute of Fisheries for cooperation in the collection of adult mussels. The authors thank 2 anonymous reviewers for their helpful comments. The first author acknowledges Japanese Ministry of Education, Culture, Sports, Science and Technology for providing a scholarship during the study period. All experiments complied with the current Japanese laws.

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Correspondence to Wei-Yang Bao.

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Communicated by S. Nishida.

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Bao, WY., Yang, JL., Satuito, C.G. et al. Larval metamorphosis of the mussel Mytilus galloprovincialis in response to Alteromonas sp. 1: evidence for two chemical cues?. Mar Biol 152, 657–666 (2007). https://doi.org/10.1007/s00227-007-0720-2

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