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Comparative analysis of biofilm community on different coloured substrata in relation to mussel settlement

Published online by Cambridge University Press:  12 February 2016

Yi-Feng Li ,
Xing-Pan Guo ,
Yu-Ru Chen ,
De-Wen Ding  and
Jin-Long Yang
Yi-Feng Li
Affiliation:
Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Ocean University, Ministry of Education, Shanghai 201306, China
Xing-Pan Guo
Affiliation:
Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Ocean University, Ministry of Education, Shanghai 201306, China
Yu-Ru Chen
Affiliation:
Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Ocean University, Ministry of Education, Shanghai 201306, China
De-Wen Ding
Affiliation:
Marine Ecology Research Center, The First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China
Jin-Long Yang*
Affiliation:
Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Ocean University, Ministry of Education, Shanghai 201306, China Marine Ecology Research Center, The First Institute of Oceanography, State Oceanic Administration, Qingdao 266061, China Collaborative Innovation Center for Zhejiang Marine High-efficiency and Healthy Aquaculture, Ningbo 315211, China
*
Correspondence should be addressed to:J.L. Yang, Key Laboratory of Exploration and Utilization of Aquatic Genetic Resources, Shanghai Ocean University, Ministry of Education, Shanghai 201306, China email: [email protected]
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Abstract

Mussels are typical macrofouling organisms in the world. In this study, the interaction between the settlement of Mytilus coruscus plantigrades and bacterial community on coloured substrata was determined. Bacterial communities in biofilms developed on seven coloured substrata were analysed by Illumina Miseq sequencing. The mussel settlement response to coloured substrata with no biofilms was also examined. Flavobacteria, Alphaproteobacteria and Gammaproteobacteria were the first, second and third most dominant groups in seven biofilm samples. The results suggest that the inducing activities of these biofilms on plantigrade settlement varied with coloured substrata and the lowest percentage of settlement was observed on biofilms on the green substratum. High-throughput sequencing showed that bacterial community in biofilms also changed with the substratum colour. No significant difference in the inducing activity on plantigrade settlement was observed between the coloured substrata with no biofilms. Thus, difference in plantigrade settlement response may be correlated to the changes in bacterial community on coloured substrata. This finding extends current knowledge of interaction among mussel settlement and bacterial community variability.

Keywords

Mytilus coruscusmussel settlementbacterial communitycoloured substrataMiseq sequencing
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 97 , Issue 1 , February 2017 , pp. 81 - 89
Copyright
Copyright © Marine Biological Association of the United Kingdom 2016 

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References

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, 269–290.Google Scholar
Alfaro, A.C., Young, T. and Ganesan, A.M. (2011) Regulatory effects of mussel (Aulacomya maoriana Iredale 1915) larval settlement by neuroactive compounds, amino acids and bacterial biofilms. Aquaculture 322–323, 158–168.Google Scholar
Allion, A., Baron, J.P. and Boulange-Petermann, L. (2006) Impact of surface energy and roughness on cell distribution and viability. Biofouling 22, 269–278.CrossRefGoogle ScholarPubMed
Alonso, C., Warnecke, F., Amann, R. and Pernthaler, J. (2007) High local and global diversity of Flavobacteria in marine plankton. Environmental Microbiology 9, 1253–1266.CrossRefGoogle ScholarPubMed
Amato, K.R., Yeoman, C.J., Kent, A., Righini, N., Carbonero, F., Estrada, A., Gaskins, H.R., Stumpf, R.M., Yildirim, S., Torralba, M., Gillis, M., Wilson, B.A., Nelson, K.E., White, B.A. and Leigh, S.R. (2013) Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. ISME Journal 7, 1344–1353.Google 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, 173–180.Google Scholar
Bao, W.Y., Satuito, C.G., Yang, J.L. and Kitamura, H. (2007) Larval settlement and metamorphosis of the mussel Mytilus galloprovincialis in response to biofilms. Marine Biology 150, 565–574.Google Scholar
Bayne, B.L. (1964) Primary and secondary settlement in Mytilus edulis L. (Mollusca). Journal of Animal Ecology 33, 513–523.Google Scholar
Bayne, B.L. (1971) Some morphological changes that occur at the metamorphosis of the larvae of Mytilus edulis . In Crisp, D.J. (ed.) Proceedings of the 4th European Marine Biological Symposium. Cambridge: Cambridge University Press, pp. 259–280.Google Scholar
Bellou, N., Papathanassiou, E., Dobretsov, S., Lykousis, V. and Colijn, F. (2012) The effect of substratum type, orientation and depth on the development of bacterial deep-sea biofilm communities grown on artificial substrata deployed in the Eastern Mediterranean. Biofouling 28, 199–213.Google Scholar
Briand, J.F. (2009) Marine antifouling laboratory bioassays: an overview of their diversity. Biofouling 25, 297–311.Google Scholar
Burke, C., Thomas, T., Lewis, M., Steinberg, P. and Kjelleberg, S. (2011) Composition, uniqueness and variability of the epiphytic bacterial community of the green alga Ulva australis . ISME Journal 5, 590–600.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, 44–56. [In Chinese with English abstract.]Google Scholar
Caporaso, J.G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F.D., Costello, E.K., Fierer, N., Pena, A.G., Goodrich, J.K., Gordon, J.I., Huttley, G.A., Kelley, S.T., Knights, D., Koenig, J.E., Ley, R.E., Lozupone, C.A., McDonald, D., Muegge, B.D., Pirrung, M., Reeder, J., Sevinsky, J.R., Tumbaugh, P.J., Walters, W.A., Widmann, J., Yatsunenko, T., Zaneveld, J. and Knight, R. (2010) QIIME allows analysis of highthroughput community sequencing data. Nature Methods 7, 335–336.Google Scholar
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, 107–117.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, 859–868.Google Scholar
Carl, C., Poole, A.J., Williams, M.R. and de Nys, R. (2012) Where to settle – settlement preferences of Mytilus galloprovincialis and choice of habitat at a micro spatial scale. PLoS One 7, e52358.Google Scholar
Chung, H.C., Lee, O.O., Huang, Y.L., Mok, S.Y., Kolter, R. and Qian, P.Y. (2010) Bacterial community succession and chemical profiles of subtidal biofilms in relation to larval settlement of the polychaete Hydroides elegans . ISME Journal 4, 817–828.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
Connell, S.D. (1999) Effects of surface orientation on the cover of epibiota. Biofouling 14, 219–226.Google Scholar
Decho, A.W. (2000) Microbial biofilms in intertidal systems: an overview. Continental Shelf Research 20, 1257–1273.Google Scholar
Dobretsov, S.V. (1999) Effects of macroalgae and biofilm on settlement of blue mussel (Mytilus edulis L.) larvae. Biofouling 14, 153–165.Google 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. 293–313.Google Scholar
Dobretsov, S., Abed, R.M.M. and Voolstra, C.R. (2013) The effect of surface colour on the formation of marine micro and macrofouling communities. Biofouling 29, 617–627.Google Scholar
Dobretsov, S.V. and Qian, P.Y. (2003) Pharmacological induction of larval settlement and metamorphosis in the blue mussel Mytilus edulis L. Biofouling 19, 57–63.Google Scholar
Fernández-Gómez, B., Richter, M., Schüler, M., Pinhassi, J., Acinas, S.G., González, J.M. and Pedrós-Alió, C. (2013) Ecology of marine bacteroidetes: a comparative genomics approach. ISME Journal 7, 1026–1037.Google Scholar
Finlay, J.A., Bennett, S.M., Brewer, L.H., Sokolova, A., Clay, G., Gunari, N., Meyer, A.E., Walker, G.C., Wendt, D.E., Callow, M.E., Callow, J.A. and Detty, M.R. (2010) Barnacle settlement and the adhesion of protein and diatom microfouling to xerogel films with varying surface energy and water wettability. Biofouling 26, 657–666.Google Scholar
Flemming, H.C. and Wingender, J. (2010) The biofilm matrix. Nature Reviews Microbiology 8, 623–633.CrossRefGoogle ScholarPubMed
Fletcher, M. and Loeb, G.I. (1979) Influence of substratum characteristics on the attachment of a marine pseudomonad to solid surfaces. Applied and Environmental Microbiology 37, 67–72.Google Scholar
Fusetani, N. (2011) Antifouling natural products. Natural Product Reports 28, 400–410.Google Scholar
Ganesan, A.M., Alfaro, A.C., Higgins, C.M., Duxbury, M. and Brooks, J.D. (2012) Characterization of biofilm exudates and their effects on settlement of mussel (Perna canaliculus) larvae. Journal of Experimental Marine Biology and Ecology 434–435, 34–46.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, 251–259.Google Scholar
Glasby, T.M. (2000) Surface composition and orientation interact to affect subtidal epibiota. Journal of Experimental Marine Biology and Ecology 248, 177–190.Google Scholar
Hadfield, M.G. (2011) Biofilms and marine invertebrate larvae: what bacteria produce that larvae use to choose settlement sites. Annual Review of Marine Science 3, 453–470.Google Scholar
Hsu, L., Fang, J., Borca-Tasciuc, D.A., Worobo, R.W. and Moraru, C.I. (2013) The effect of micro- and nanoscale topography on the adhesion of bacterial cells to solid surfaces. Applied and Environmental Microbiology 79, 2703–2712.Google Scholar
Huang, S. and Hadfield, M.G. (2003) Composition and density of bacterial biofilms determine larval settlement of the polychaete Hydroides elegans . Marine Ecology Progress Series 260, 161–172.CrossRefGoogle Scholar
Huang, Y., Callahan, S. and Hadfield, M.G. (2012) Recruitment in the sea: bacterial genes required for inducing larval settlement in a polychaete worm. Scientific Reports 2, 228.CrossRefGoogle 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, 387–399.Google Scholar
James, R.J. and Underwood, A.J. (1994) Influence of colour of substratum on recruitment of spirorbid tubeworms to different types of intertidal boulders. Journal of Experimental Marine Biology and Ecology 181, 105–115.Google Scholar
Jones, P.R., Cottrell, M.T., Kirchman, D.L. and Dexter, S.C. (2007) Bacterial community structure of biofilms on artificial surfaces in an estuary. Microbial Ecology 53, 153–162.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, 247–256.CrossRefGoogle ScholarPubMed
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, 153–163.Google Scholar
Kon-ya, K. and Miki, W. (1994) Effects of environmental factors on larval settlement of the barnacle Balanus amphitrite reared in the laboratory. Fisheries Science 60, 563–565.Google Scholar
Lau, S.C.K., Thiyagarajan, V., Cheung, S.C.K. and Qian, P.Y. (2005) Roles of bacterial community composition in biofilms as a mediator for larval settlement of three marine invertebrates. Aquatic Microbial Ecology 38, 41–51.CrossRefGoogle Scholar
Lee, O.O., Wang, Y., Yang, J., Lafi, F.F., Al-Suwailem, A. and Qian, P.Y. (2011) Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea. ISME Journal 5, 650–664.Google Scholar
Li, Y.F., Chen, Y.R., Yang, J.L., Bao, W.Y., Guo, X.P., Liang, X., Shi, Z.Y., Li, J.L. and Ding, D.W. (2014) Effects of substratum type on bacterial community structure in biofilms in relation to settlement of plantigrades of the mussel Mytilus coruscus . International Biodeterioration Biodegradation 96, 41–49.CrossRefGoogle Scholar
Nasrolahi, A., Stratil, S.B., Jacob, K.J. and Wahl, M. (2012) A protective coat of microorganisms on macroalgae: inhibitory effects of bacterial biofilms and epibiotic microbial assemblages on barnacle attachment. FEMS Microbiology Ecology 81, 583–595.Google Scholar
Palmer, R.J. and White, D.C. (1997) Developmental biology of biofilms: implications for treatment and control. Trends in Microbiology 5, 435–440.Google Scholar
Patel, P., Callow, M.E., Joint, I. and Callow, J.A. (2003) Specificity in the settlement – modifying response of bacterial biofilms towards zoospores of the marine alga Enteromorpha . Environmental Microbiology 5, 338–349.Google Scholar
Petrone, L. (2013) Molecular surface chemistry in marine bioadhesion. Advances in Colloid and Interface Science 195–196, 1–18.Google Scholar
Pomerat, C.M. and Reiner, E.R. (1942) The influence of surface angle and of light on the attachment of barnacles and other sedentary organisms. Biological Bulletin 82, 14–25.CrossRefGoogle Scholar
Prendergast, G.S. (2010) Settlement and behavior of marine fouling organisms. In Dürr, S. and Thomason, J.C. (eds) Biofouling. Oxford: Wiley-Blackwell, pp. 30–51.Google Scholar
Qian, P.Y. and Dahm, H.U. (2009) A triangle model: environmental changes affect biofilms that affect larval setlement. In Flemming, H.C., Murthy, P.S., Venkatesan, R. and Cooksey, K. (eds) Marine and industrial biofouling. Berlin: Springer-Verlag, pp. 315–328.Google Scholar
Qian, P.Y., Thiyagarajan, V., Lau, S.C.K. and Cheung, S.C.K. (2003) Relationship between bacterial community profile in biofilm and attachment of the acorn barnacle Balanus amphitrite . Aquatic Microbial Ecology 33, 225–237.Google Scholar
Qian, P.Y., Wang, Y., Lee, O.O., Lau, S.C., Yang, J., Lafi, F.F., Al-Suwailem, A. and Wong, T.Y. (2011) Vertical stratification of microbial communities in the Red Sea revealed by 16S rDNA pyrosequencing. ISME Journal 5, 507–518.Google Scholar
Robson, M.A., Williams, D., Wolff, K. and Thomason, J.C. (2009) The effect of surface colour on the adhesion strength of Elminius modestus Darwin on a commercial non-biocidal antifouling coating at two locations in the UK. Biofouling 25, 215–227.Google Scholar
Satuito, C.G., Natoyama, K., Yamazaki, M. and Fusetani, N. (1995) Induction of attachment and metamorphosis of laboratory cultured mussel Mytilus edulis galloprovincialis larvae by microbial film. Fisheries Science 61, 223–227.Google Scholar
Saucedo, P.E., Bervera-Leon, H., Monteforte, M., Southgate, P.C. and Monsalvo-Spencer, P. (2005) Factors influencing recruitment of hatchery reared pearl oyster (Pinctada mazatlanica; Hanley 1856) spat. Journal of Shellfish Research 24, 215–219.Google Scholar
Satheesh, S. and Wesley, S.G. (2010) Influence of substratum colour on the recruitment of macrofouling communities. Journal of the Marine Biological Association of the United Kingdom 90, 941–946.Google Scholar
Scardino, A.J. and de Nys, R. (2011) Mini review: biomimetic models and bioinspired surfaces for fouling control. Biofouling 27, 73–86.Google Scholar
Seed, R. (1969) The ecology of Mytilus edulis L. (Lamellibranchiata) on the exposed rocky shores. I. Breeding and settlement. Oecologia (Berlin) 3, 277–316.Google Scholar
Sharp, K.H., Distel, D. and Paul, V.J. (2012) Diversity and dynamics of bacterial communities in early life stages of the Caribbean coral Porites astreoides . ISME Journal 6, 790–801.Google Scholar
Shikuma, N.J. and Hadfield, M.G. (2010) Marine biofilms on submerged surfaces are a reservoir for Escherichia coli and Vibrio cholerae . Biofouling 26, 39–46.Google Scholar
Swain, G., Herpe, S., Ralston, E. and Tribou, M. (2006) Short-term testing of antifouling surfaces: the importance of colour. Biofouling 22, 425–429.Google Scholar
Thiyagarajan, V., Lau, S.C.K., Cheung, S.C.K. and Qian, P.Y. (2006) Cypris habitat selection facilitated by microbial films influences the vertical distribution of subtidal barnacle Balanus trigonus . Microbial Ecology 51, 431–440.Google Scholar
Thomas, T., Evans, F.F., Schleheck, D., Mai-Prochnow, A., Burke, C., Penesyan, A., Dalisay, D.S., Stelzer-Braid, S., Saunders, N., Johnson, J., Ferriera, S., Kjelleberg, S. and Egan, S. (2008) Analysis of the Pseudoalteromonas tunicata genome reveals properties of a surface-associated life style in the marine environment. PLoS One 3, e3252.Google Scholar
Tran, C. and Hadfield, M.G. (2011) Larvae of Pocillopora damicornis (Anthozoa) settle and metamorphose in response to surface-biofilm bacteria. Marine Ecology Progress Series 433, 85–96.Google Scholar
Unabia, C.R.C. and Hadfield, M.G. (1999) Role of bacteria in larval settlement and metamorphosis of the polychaete Hydroides elegans . Marine Biology 133, 55–64.Google Scholar
Verran, J. and Boyd, R.D. (2001) The relationship between substratum surface roughness and microbiological and organic soiling: a review. Biofouling 17, 59–71.Google Scholar
Vrolijk, N.H., Targett, N.M., Baier, R.E. and Meyer, A.E. (1990) Surface characterisation of two gorgonian coral species: implications for a natural antifouling defence. Biofouling 2, 39–54.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, 1–21.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, 249–256.CrossRefGoogle ScholarPubMed
Whitehead, K.A. and Verran, J. (2009) The effect of substratum properties on the survival of attached microorganisms on inert surfaces. In Flemming, H.C., Murthy, P.S., Venkatesan, R. and Cooksey, K. (eds) Marine and industrial biofouling. Berlin: Springer-Verlag, pp. 13–33.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, 81–118.Google Scholar
Yang, J.L., Li, S.H., Li, Y.F., Liu, Z.W., Liang, X., Bao, W.Y. and Li, J.L. (2013a) Effects of neuroactive compounds, ions and organic solvents on larval metamorphosis of the mussel Mytilus coruscus . Aquaculture 396–399, 106–112.CrossRefGoogle 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, 193–199.Google Scholar
Yang, J.L., Satuito, C.G., Bao, W.Y. and Kitamura, H. (2007) Larval settlement and metamorphosis of the mussel Mytilus galloprovincialis on different macroalgae. Marine Biology 152, 1121–1132.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, 461–470.Google Scholar
Yang, J.L., Shen, P.J., Liang, X., Li, Y.F., Bao, W.Y. and Li, J.L. (2013b) Larval settlement and metamorphosis of the mussel Mytilus coruscus in response to monospecific bacterial biofilms. Biofouling 29, 247–259.Google Scholar
Yang, J.L., Zhou, X., Li, Y.F., Guo, X.P., Liang, X. and Li, J.L. (2014) Plantigrade settlement of the mussel Mytilus coruscus in response to natural biofilms on different surfaces. Journal of the Marine Biological Association of the United Kingdom 94, 1639–1649.Google Scholar
Young, T., Alfaro, A.C. and Robertson, J. (2011) Effect of neuroactive compounds on the settlement of mussel (Perna canaliculus). Aquaculture 319, 277–283.Google Scholar
Yule, A.B. and Walker, G. (1984) The temporary adhesion of barnacle cyprids: effects of some differing surface characteristics. Journal of the Marine Biological Association of the United Kingdom 64, 429–439.Google Scholar
Zobell, C.E. and Allen, E.C. (1935) The significance of marine bacteria in the fouling of submerged surfaces. Journal of Bacteriology 29, 239–251.Google Scholar
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