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Plantigrade settlement of the mussel Mytilus coruscus in response to natural biofilms on different surfaces

  • Jin-Long Yang (a1) (a2) (a3), Xuan Zhou (a1), Yi-Feng Li (a1), Xing-Pan Guo (a1), Xiao Liang (a1) and Jia-Le Li (a1)...

Abstract

Surface properties affect the attachment of micro- and macroscopic marine organisms. The current study examined the settlement response of the mussel Mytilus coruscus plantigrades to natural biofilms formed on surfaces of different wettability. The percentages of plantigrade settlement were not influenced by the biofilms formed on variously wettable surfaces in the short term, but after 10 days, the plantigrade settlement rates decreased on biofilms formed on lower wettability surfaces. In general, lower wettability of the surfaces resulted in the decrease of the dry weight, bacterial and diatom density and the thickness of natural biofilms when compared to high wettability surfaces. In contrast, chlorophyll-a concentration in biofilms was independent of the initial wettability of the surfaces. Comparative cluster analysis of bacterial denaturing gradient gel electrophoresis patterns revealed that high variability existed between the bacterial community on high wettability surfaces and that on low wettability surfaces. Thus, surface wettability affects the formation of natural biofilms, and this variation in biofilms developed on different wettability surfaces may explain the discrepancy in their corresponding inducing activities on M. coruscus plantigrade settlement. This finding provides new insight into interactions between mussel settlement, biofilm characteristics and surface properties.

Copyright

Corresponding author

Correspondence should be addressed to: J.L. Yang, College of Fisheries and Life Science, Shanghai Ocean UniversityShanghai 201306, China email: jlyang@shou.edu.cn

References

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Alfaro, A.C., Jeffs, A.G. and Creese, R.G. (2004) Bottom-drifting algal/mussel spat associations along a sanday coastal region in northern New Zealand. Aquaculture 241, 269290.
Ank, G., Porto, T.F., Pereira, R.C. and da Gama, B.A.P. (2009) Effects of different biotic substrata on mussel attachment. Biofouling 25, 173180.
Bao, W.Y., Satuito, C.G., Yang, J.L. and Kitamura, H. (2007a) Larval settlement and metamorphosis of the mussel Mytilus galloprovincialis in response to biofilms. Marine Biology 150, 565574.
Bao, W.Y., Yang, J.L., Satuito, C.G. and Kitamura, H. (2007b) Larval metamorphosis of the mussel Mytilus galloprovincialis in response to Alteromonas sp. 1: evidence for two chemical cues? Marine Biology 152, 657666.
Bayne, B.L. (1964) Primary and secondary settlement in Mytilus edulis L. (Mollusca). Journal of Animal Ecology 33, 513523.
Cai, R.X., Chen, S.Q., Xue, J.Z. and Lu, J.P. (1994) The ecology of fouling organism in Gouqi waters, Zhoushan. Donghai Marine Science 12, 4456. [In Chinese with English Abstract.]
Callow, J.A. and Callow, M.E. (2011) Trends in the development of environmentally friendly fouling-resistant marine coatings. Nature Communication 2, 244.
Campbell, A.H., Meritt, D.W., Franklin, R.B., Boone, E.L., Nicely, C.T. and Brown, B.L. (2011) Effects of age and composition of field-produced biofilms on oyster larval setting. Biofouling 27, 255265.
Cárceres-Martínez, J., Robledo, J.A.F. and Figueras, A. (1994) Settlement and post-larvae behaviour of Mytilus galloprovinvialis: field and laboratory experiments. Marine Ecology Progress Series 112, 107117.
Carl, C., Poole, A.J., Sexton, B.A., Glenn, F.L., Vucko, M.J., Williams, M.R., Whalan, S. and de Nys, R. (2012) Enhancing the settlement and attachment strength of pediveligers of Mytilus galloprovincialis bychanging surface wettability and microtopography. Biofouling 28, 175186.
Carl, C., Poole, A.J., Vucko, M.J., Williams, M.R., Whalan, S. and de Nys, R. (2011) Optimising settlement assays of pediveligers and plantigrades of Mytilus galloprovincialis. Biofouling 27, 859868.
Chang, Y.Q. (2007) Stock enhancement and culture in mollusks. Beijing: China Agriculture Press. [In Chinese.]
Clarke, K.R. and Warwick, R.M. (2001) Change in marine communities: an approach to statistical analysis and interpretation. Plymouth: Plymouth Marine Laboratory.
Dahlström, M., Jonsson, H., Jonsson, P.R. and Elwing, H. (2004) Surface wettability as a determinant in the settlement of the barnacle Balanus Improvisus (DARWIN). Journal of Experimental Marine Biology and Ecology 305, 223232.
Dalton, H.M., Poulsen, L.K., Halasz, P., Angles, M.L., Goodman, A.E. and Marshall, K.C. (1994) Substratum-induced morphological changes in a marine bacterium and their relevance to biofilm structure. Journal of Bacteriology 176, 69006906.
Dobretsov, S. (2009) Inhibition and induction of marine biofouling by biofilms. In Flemming, H.C., Murthy, P.S., Venkatesan, R. and Cooksey, K. (eds) Marine and industrial biofouling. Berlin: Springer-Verlag, pp. 293313.
Dobretsov, S. (2010) Marine biofilms. In Dürr, S. and Thomason, J.C. (eds) Biofouling. Oxford: Wiley-Blackwell, pp. 123136.
Dobretsov, S., Abed, R.M.M. and Teplitski, M. (2013) Mini-review: inhibition of biofouling by marine microorganisms. Biofouling 29, 423441.
Dobretsov, S. and Qian, P.Y. (2004) The role of epibotic bacteria from the surface of the soft coral Dendronephthya sp. in the inhibition of larval settlement. Journal of Experimental Marine Biology and Ecology 299, 3550.
Faimali, M., Garaventa, F., Terlizzi, A., Chiantore, M. and Cattaneo-Vietti, R. (2004) The interplay of substrate nature and biofilm formation in regulating Balanus amphitrite Darwin, 1854 larval settlement. Journal of Experimental Marine Biology and Ecology 306, 3750.
Finlay, J.A., Callow, M.E., Ista, L.K., Lopez, G.P. and Callow, J.A. (2002) The influence of surface wettability on the adhesion strength of settled spores of the green alga Enteromorpha and the diatom Amphora. Integrative and Comparative Biology 42, 11161122.
García-Fernández, L., Cui, J., Serrano, C., Gropeanu, R.A., San Miguel, V., Iturri Ramos, J., Wang, M., Auernhammer, G.K., Ritz, S., Golriz, A.A., Berger, R., Wagner, M. and del Campo, A. (2013) Antibacterial strategies from the sea: polymer-bound Cl-catechols for prevention of biofilm formation. Advanced Materials 25, 529533.
Genzer, J. and Efimenko, K. (2006) Recent developments in superhydrophobic surfaces and their relevance to marine fouling: a review. Biofouling 22, 339360.
Gerhart, D.J., Rittschof, D., Hooper, I.R. and Eisenman, K. (1992) Rapid and inexpensive quantification of the combined polar components of surface wettability: application to biofouling. Biofouling 5, 251259.
Henschel, J.R. and Cook, P.A. (1990) The development of a marine fouling community in relation to the primary film of microorganisms. Biofouling 2, 111.
Holland, R., Dugdale, T.M., Wetherbee, R., Brennan, A.B., Finlay, J.A., Callow, J.A. and Callow, M.E. (2004) Adhesion and motility of fouling diatoms on a silicone elastomer. Biofouling 20, 323329.
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, 21112115.
Huggett, M.J., Nedved, B.T. and Hadfield, M.G. (2009) Effects of initial surface wettability on biofilm formation and subsequent settlement of Hydroides elegans. Biofouling 25, 387399.
Hung, Q.S., Thiyagarajan, V. and Qian, P.Y. (2008) Preferential attachment of barnacle larvae to natural multi-species biofilms: does surface wettability matter? Journal of Experimental Marine Biology and Ecology 361, 3641.
Kavouras, J. and Maki, J. (2003) The effects of natural biofilms on the reattachment of young adult zebra mussels to artificial substrata. Biofouling 19, 247256.
Kirchman, D., Graham, S., Reish, D. and Mitchell, R. (1982) Bacteria induce settlement and metamorphosis of Janua (Dexiospira) brasiliensis Grube (Polychaeta: Spirorbidae). Journal of Experimental Marine Biology and Ecology 56, 153163.
Ma, M.Y., Liu, J.L. and Wang, X.M. (2011) Biofilms as potential indicators of macrophyte-dominated lake health. Ecotoxicology 20, 982992.
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, 159170.
Maki, J.S., Rittschof, D., Samuelsson, M.Q., Szewzyk, U., Yule, A.B., Kjelleberg, S., Costlow, J.D. and Mitchell, R. (1990) Effect of marine bacteria and their exopolymers on the attachment of barnacle cypris larvae. Bulletin of Marine Science 46, 499511.
Muyzer, G., de Waal, E.C. and Uitterlinden, A.G. (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Applied and Environmental Microbiology 59, 695700.
Petrone, L. (2013) Molecular surface chemistry in marine bioadhesion. Advances in Colloid and Interface Science 195–196, 118.
Prendergast, G.S. (2010) Settlement and behaviour of marine fouling organisms. In Dürr, S. and Thomason, J.C. (eds) Biofouling. Oxford: Wiley-Blackwell, pp. 3051.
Rittschof, D. and Costlow, J.D. (1989) Bryozoan and barnacle settlement in relation to initial surface wettability: a comparison of laboratory and field studies. Scientia Marina 53, 411416.
Terlizzi, A. and Faimali, M. (2010) Fouling on artificial substrata. In Dürr, S. and Thomason, J.C. (eds) Biofouling. Oxford: Wiley-Blackwell, pp. 170184.
Thompson, R.C., Tobin, M.L., Hawkins, S.J. and Norton, T.A. (1999) Problems in extraction and spectrophotometric determination of chlorophyll from epilithic microbial biofilms: towards a standard method. Journal of the Marine Biological Association of the United Kingdom 79, 551558.
Thompson, S.E., Taylor, A.R., Brownlee, C., Callow, M.E. and Callow, J.A. (2008) The role of nitric oxide in diatom adhesion in relation to substratum properties. Journal of Phycology 44, 967976.
Toupoint, N., Mohit, V., Linossier, I., Bourgougnon, N., Myrand, B., Olivier, F., Lovejoy, C. and Tremblay, R. (2012) Effect of biofilm age on settlement of Mytilus edulis. Biofouling 28, 9851001.
von der Meden, C.E.O., Porri, F., McQuaid, C.D., Faulkner, K. and Robey, J. (2010) Fine-scale ontogenetic shifts in settlement behaviour of mussels: changing responses to biofilm and conspecific settler presence in Mytilus galloprovincialis and Perna perna. Marine Ecology Progress Series 411, 161171.
Wahl, M., Goecke, F., Labes, A., Dobretsov, S. and Weinberger, F. (2012) The second skin: ecological role of epibiotic biofilms on marine organisms. Frontiers in Microbiology 3, 121.
Wang, C., Bao, W.Y., Gu, Z.Q., Li, Y.F., Liang, X., Ling, Y., Cai, S.L., Shen, H.D. and Yang, J.L. (2012) Larval settlement and metamorphosis of the mussel Mytilus coruscus in response to natural biofilms. Biofouling 28, 249256.
Wieczorek, S.K. and Todd, C.D. (1998) Inhibition and facilitation of settlement of epifaunal marine invertebrate larvae by microbial biofilm cues. Biofouling 12, 81118.
Yang, J.L., Li, X., Liang, X., Bao, W.Y., Shen, H.D. and Li, J.L. (2014) Effects of natural biofilms on settlement of plantigrades of the mussel Mytilus coruscus. Aquaculture 424–425, 228233.
Yang, J.L., Li, Y.F., Satuito, C.G., Bao, W.Y. and Kitamura, H. (2011) Larval metamorphosis of the mussel Mytilus galloprovincialis Lamarck, 1819 in response to neurotransmitter blockers and tetraethylammonium. Biofouling 27, 193199.
Yang, J.L., Satuito, C.G., Bao, W.Y. and Kitamura, H. (2008) Induction of metamorphosis of pediveliger larvae of the mussel Mytilus galloprovincialis Lamarck, 1819 using neuroactive compounds, KCl, NH4Cl and organic solvents. Biofouling 24, 461470.
Yang, J.L., Shen, P.J., Liang, X., Li, Y.F., Bao, W.Y. and Li, J.L. (2013) Larval settlement and metamorphosis of the mussel Mytilus coruscus in response to monospecific bacterial biofilms. Biofouling 29, 247259.
Yu, X.J., He, W.H., Li, H.X., Yan, Y. and Lin, C.X. (2010) Larval settlement and metamorphosis of the pearl oyster Pinctada fucata in response to biofilms. Aquaculture 306, 334337.

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