Hostname: page-component-848d4c4894-sjtt6 Total loading time: 0 Render date: 2024-06-25T16:10:45.009Z Has data issue: false hasContentIssue false

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

Published online by Cambridge University Press:  30 July 2014

Jin-Long Yang*
Affiliation:
College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, China Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Ocean University, Ministry of Education, Shanghai 201306, China Shanghai University Knowledge Service Platform, Shanghai Ocean University Aquatic Animal Breeding Center (ZF1206), Shanghai 201306, China
Xuan Zhou
Affiliation:
College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, China
Yi-Feng Li
Affiliation:
College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, China
Xing-Pan Guo
Affiliation:
College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, China
Xiao Liang
Affiliation:
College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, China
Jia-Le Li
Affiliation:
College of Fisheries and Life Science, Shanghai Ocean University, Shanghai 201306, China
*
Correspondence should be addressed to: J.L. Yang, College of Fisheries and Life Science, Shanghai Ocean UniversityShanghai 201306, China email: jlyang@shou.edu.cn

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.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Bayne, B.L. (1964) Primary and secondary settlement in Mytilus edulis L. (Mollusca). Journal of Animal Ecology 33, 513523.Google Scholar
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.]Google Scholar
Callow, J.A. and Callow, M.E. (2011) Trends in the development of environmentally friendly fouling-resistant marine coatings. Nature Communication 2, 244.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.Google Scholar
Chang, Y.Q. (2007) Stock enhancement and culture in mollusks. Beijing: China Agriculture Press. [In Chinese.]Google Scholar
Clarke, K.R. and Warwick, R.M. (2001) Change in marine communities: an approach to statistical analysis and interpretation. Plymouth: Plymouth Marine Laboratory.Google Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
Dobretsov, S. (2010) Marine biofilms. In Dürr, S. and Thomason, J.C. (eds) Biofouling. Oxford: Wiley-Blackwell, pp. 123136.Google Scholar
Dobretsov, S., Abed, R.M.M. and Teplitski, M. (2013) Mini-review: inhibition of biofouling by marine microorganisms. Biofouling 29, 423441.Google Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
Genzer, J. and Efimenko, K. (2006) Recent developments in superhydrophobic surfaces and their relevance to marine fouling: a review. Biofouling 22, 339360.Google Scholar
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.CrossRefGoogle Scholar
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.CrossRefGoogle Scholar
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.CrossRefGoogle Scholar
Ma, M.Y., Liu, J.L. and Wang, X.M. (2011) Biofilms as potential indicators of macrophyte-dominated lake health. Ecotoxicology 20, 982992.CrossRefGoogle ScholarPubMed
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.Google Scholar
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.Google Scholar
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.Google Scholar
Petrone, L. (2013) Molecular surface chemistry in marine bioadhesion. Advances in Colloid and Interface Science 195–196, 118.Google Scholar
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.Google Scholar
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.Google Scholar
Terlizzi, A. and Faimali, M. (2010) Fouling on artificial substrata. In Dürr, S. and Thomason, J.C. (eds) Biofouling. Oxford: Wiley-Blackwell, pp. 170184.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar
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.Google Scholar