Abstract
In this work, 37 bacterial strains isolated from biofouling of marine organisms and from the Museum of Heterotrophic Bacteria of the National Scientific Center of Marine Biology were studied. The strains were identified based on their phenotypic characteristics and on the fatty acid composition of their cell wall lipids. Members of the genus Pseudoalteromonas prevailed both in associated microflora of two dinoflagellate clones and in the biofilms from marine hydrobionts. Associated microflora included also members of the CFB cluster, Bacillus, Sulfitobacter, Acinetobacter, Shewanella, and Psychrobacter. A considerable portion of strains (48.6%) exhibited antimicrobial activity. Antifouling activity against algal spores was studied using single-species bacterial biofilms and the spores of Ulva lactuca и Undaria pinnatifida, the algae most common in the Sea of Japan. Strong inhibitory effect on attachment of Ulva and Undaria spores was observed for 75 and 51% of the strains, respectively. Attached spores were, however, less sensitive to the inhibitory action of biofilms. Species specificity of algal response to bacteria was shown, with a strain having different effect on the spores of different algal species. Biotechnologically promising strains were determined, which exhibited high activity against the spores of macroalgae and could probably be used as producers of antifouling substances and as components of antifouling coatings. No relation was found between antifouling activity of bacteria and the source of their isolation. Our results indicate wide occurrence of bacteria with antifouling activity among associated microflora of marine hydrobionts and demonstrate the extent of complexity and diversity of relations between bacterial biofilms and algal spores.
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Beleneva, I.A., Dautova, T.N., and Zhukova, N.V, Characterization of communities of heterotrophic bacteria associated with healthy and diseased corals in Nha Trang Bay (Vietnam), Microbiology (Moscow), 2005, vol. 74, no. 5, pp. 579–587.
Beleneva, I.A., Magarlamov, T.Yu., and Kukhlevsky, A.D, Characterization, identification, and screening for tetrodotoxin production by bacteria associated with the ribbon worm (Nemertea) Cephalotrix simula (Ivata, 1952), Microbiology (Moscow), 2014, vol. 83, no. 3, pp. 220–226.
Beleneva, I.A., Kukhlevsky, A.D., and Kharchenko, U.V, Antimicrobial activity of heterotrophic bacterial strains of marine origin, Jundishapur J. Microbiol., 2013, vol. 6, pp. 166–175.
Bernbom, N., Ng, Y.Y., Kjelleberg, S., Harder, T., and Gram, L, Marine bacteria from Danish coastal waters show antifouling activity against the marine fouling bacterium Pseudoalteromonas sp. strain S91 and zoospores of the green alga Ulva australis independent of bacteriocidal activity, Appl. Environ. Microbiol., 2011, vol. 77, pp. 8557–8567.
Bowman, J.P., Nichols, D.S., and McMeekin, T.A, Psychrobacter glacincola sp. nov., a halotolerant, psychrophilic bacterium isolated from Antarctic sea ice, Syst. Appl. Microbiol., 1997, vol. 20, pp. 209–215.
Dillon, P.S., Maki, J.S., and Mitchell, R, Adhesion of Enteromorpha swarmers to microbial films, Microb. Ecol., 1989, vol. 17, pp. 39–47.
Dobretsov, S.V., Dahms, H.U., and Qian, P.Y, Inhibition of biofouling by marine microorganisms and their metabolites, Biofouling, 2006, vol. 22, pp. 43–54.
Dobretsov, S., Abed, R.M.M., and Teplitski M, Minireview: inhibition of biofouling by marine microorganisms, Biofouling, 2013, vol. 29, pp. 423–441.
Egan, S., Thomas, T, Holmström, C., and Kjelleberg, S., Phylogenetic relationship and antifouling activity of bacterial epiphytes from the marine alga Ulva lactuca, Environ. Microbiol., 2000, vol. 2, pp. 343–347.
Egan, S, Holmström, C., and Kjelleberg, S., Pseudoalteromonas ulvae sp. nov. bacterium with antifouling activity isolated from the surface of a marine alga, Int. J. Syst. Evol. Microbiol., 2001, vol. 51, pp. 1499–1504.
Egan, S., James, S., and Kjelleberg, S, Identification and characterization of a putative transcriptional regulator controlling the expression of fouling inhibitors in Pseudoalteromonas tunicate, Appl. Environ. Microbiol., 2002, vol. 68, pp. 372–378.
Fautz, E., Rosenfelder, G., and Grotjahn, L., iso-Branched 2-and 3-hydroxy fatty acids as characteristic lipid constituents of some gliding bacteria, J. Bacteriol., 1979, vol. 140, pp. 852–858.
Fenical, W. and Jensen, P.R., Enzyme inhibitors and other bioactive compounds from marine actinomycetes, in Marine Biotechnology, Attaway, D. and Zaborsky, O., Eds., New York: Plenum,1993, vol. 1, pp. 419–457.
Huang, Y.L., Ki, J.S., Case, R.J., and Qian, P.Y, Diversity and acyl-homoserine lactone production among subtidal biofilm-forming bacteria, Aquat. Microb. Ecol., 2008, vol. 52, pp. 185–193.
Huang, Y.L., Li, M., Yu, Z.L., and Qian, P.Y, Correlation between pigmentation and larval settlement deterrence by Pseudoalteromonas sp. sf57, Biofouling, 2011, vol. 27, pp. 287–293.
Ivanova, E.P., Zhukova, N.V., Svetashev, V.I., Gorshkova, N.M., Kurilenko, V.V., Frolova, G.M., and Mikhailov, V.V, Evaluation of phospholipid and fatty acid compositions as chemotaxonomic markers of Alteromonaslike proteobacteria, Curr. Microbiol., 2000, vol. 41, pp. 341–345.
Kampfer, P, Grouping of Acinetobacter genomic species by cellular fatty acids composition, Med. Microbiol. Lett., 1993, vol. 2, pp. 394–400.
Lee, O.O., Lau, S.C.K., Tsoi, M.M.Y., Li X., Plakhotnikova, I., Dobretsov, S., Wu, M.C.S., Wong, P.-K., Weinbauer, M., and Qian, P.-Y., Shewanella irciniae sp. nov., a novel member of the family Shewanellaceae, isolated from the marine sponge Ircinia dendroides in the Bay of Villefranche, Mediterranean Sea, Int. J. Syst. Evol. Microbiol., 2006, vol. 56, pp. 2871–2877.
Li, D., Zhang, H., Fu, L., An, H., Zhang, B., Li, Y., Chen, Z., Zheng, W., Yi, L., and Zheng, T., A novel algicide: evidence of the effect of a fatty acid compound from the marine bacterium, Vibrio sp. BS02 on the harmful Dinoflagellate, Alexandrium tamarense, PLoS One, 2014, vol. 9, no. 3. e91201.
Long, R.A. and Azam, F, Antagonistic interactions among marine pelagic bacteria, Appl. Environ. Microbiol., 2001, vol. 67, pp. 4975–4983.
Lovejoy, C., Bowman, J., and Hallegraeff, G, Algicidal effects of a novel marine Pseudoalteromonas isolate (class Proteobacteria, ?-subdivision), App. Environ. Microbiol., 1998, vol. 64, pp. 2806–2813.
Ma, Y.X., Liu, P.L., Yu, S., Li, D.T., and Cao, S.M, Inhibition of common fouling organisms in mariculture by epiphytic bacteria from the surfaces of seaweeds and invertebrates, Acta Ecol. Sin., 2009, vol. 29, pp. 222–226.
Maki, J.S., Rittschof, D., Costlow, J.D., and Mitchell, R, Inhibition of attachment of larval barnacles, Balanus amphitrite, by bacterial surface films, Mar. Biol., 1988, vol. 97. 199–206.
Mieszkin, S., Callow, M.E., and Callow, J.A, Interactions between microbial biofilms and marine fouling algae: a mini review, Biofouling, 2013, vol. 29, pp. 1097–1113.
Patel, P., Callow, M.E., Joint, I., and Callow, J.A, Specificity in the settlement–modifying response of bacterial biofilms towards zoospores of the marine alga Enteromorpha, Environ. Microbiol., 2003, vol. 5, pp. 338–349.
Pukall, R, Buntefuß, D., Frühling, A., Rohde, M., Kroppenstedt, R. M. Burghardt, J., Lebaron, P., Bernard, L., and Stackebrandt, E. Sulfitobacter mediterraneus sp. nov., a new sulfite-oxidizing member of the a-Proteobacteria, Int. J. Syst. Bacteriol., 1999, vol. 49, pp. 513–519.
Qian, P.-Y., Lau, S.C.K., Dahms, H-U., Dobretsov, S., and Harder, T, Marine biofilm as mediator of colonization by marine macroorganisms: implications for antifouling and aquaculture, Marine Biotechnol., 2007, vol. 9, pp. 399–410.
Rao, D., Webb, J.S, Holmström, C., Case, R., Low, A., Steinberg, P., and Kjelleberg, S, Low densities of epiphytic bacteria from the marine alga Ulva australis inhibit settlement of fouling organisms, Appl. Envir. Microbiol., 2007, vol. 73, pp. 7844–7852.
Szewzyk, U., Holmström, C., Wrangstadh, M., Samuelsson, M.-O., Maki, J.S., and Kjelleberg, S, Relevance of the exopolysaccharide of marine Pseudomonas sp. strain S9 for the attachment of Ciona intestinalis larvae, Mar. Ecol. Prog. Ser., 1991, vol. 75, pp. 259–265.
Tait, K., Joint, I., Daykin, M., Milton, D.L., Williams, P., and Cámara, M, Disruption of quorum sensing in seawater abolishes attraction of zoospores of the green alga Ulva to bacterial biofilms, Environ. Microbiol., 2005, vol. 7, pp. 229–240.
Techniques for Corrosion Monitoring, Yang, L., Ed., Elsevier, 2008.
Yebra, D.M., Kiil, S., Weinell, C.E., and Dam-Johansen, K, Presence and effects of marine microbial biofilms on biocide-based antifouling paints, Biofouling, 2006, vol. 22, pp. 33–41.
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Original Russian Text © I.A. Beleneva, A.V. Skriptsova, V.I. Svetashev, 2017, published in Mikrobiologiya, 2017, Vol. 86, No. 3, pp. 292–306.
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Beleneva, I.A., Skriptsova, A.V. & Svetashev, V.I. Characterization of biofilm-forming marine bacteria and their effect on attachment and germination of algal spores. Microbiology 86, 317–329 (2017). https://doi.org/10.1134/S0026261717030031
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DOI: https://doi.org/10.1134/S0026261717030031