Phylogenetic analysis and antibiotic activity of bacteria isolated from the surface of two co-occurring macroalgae from the Baltic Sea

European Journal of Phycology

Volumn 48, Issue 1, 2013, Pages 47-60

  Goecke, Franz ^a   Labes, Antje ^a   Wiese, Jutta ^a   Imhoff, Johannes F ^a  

^a GEOMAR HELMHOLTZ CENTRE FOR OCEAN RESEARCH KIEL   (Germany)

Author keywords

antimicrobial activities; bacterial cultures; chemical associations; Delesseria; epiphytic bacteria; Fucus; Kiel; macroalga bacteria associations

Indexed keywords

COMPARATIVE STUDY; GROWTH RATE; MACROALGA; METABOLITE; MICROBIAL ACTIVITY; PATHOGEN; PHYLOGENETICS; RNA; SEAWATER;

ATLANTIC OCEAN; BALTIC SEA; GERMANY; KIEL FJORD; SCHLESWIG-HOLSTEIN;

ACTINOBACTERIA; ALGAE; ALGICOLA BACTERIOLYTICA; ALPHAPROTEOBACTERIA; BACILLI (CLASS); BACILLUS (BACTERIUM); BACILLUS ALGICOLA; BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); BETAPROTEOBACTERIA; CANDIDA GLABRATA; DELESSERIA; DELESSERIA SANGUINEA; ESCHERICHIA COLI; FLAVOBACTERIA; FORMOSA ALGAE; FUCUS; FUCUS VESICULOSUS; GAMMAPROTEOBACTERIA; PSEUDOALTEROMONAS; PSEUDOALTEROMONAS ELYAKOVII; STAPHYLOCOCCUS LENTUS;

EID: 84875950925     PISSN: 09670262     EISSN: 14694433     Source Type: Journal    
DOI: 10.1080/09670262.2013.767944     Document Type: Article

References (77)

1. Akagawa-Matsushita, M., Matsuo, M., Koga, Y. and YAMASATo, K. 1992. Alteromonas atlantica sp. nov. and Alteromonas carrageenovora sp. nov., bacteria that decompose algal polysaccharides. International Journal of Systematic Bacteriology, 42: 621-627.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. 1990. Basic local alignment search tool. Journal of Molecular Biology, 215: 403-410.
3. Armstrong, E., Yan, L., Boyd, K.G., Wright, P.C. and Burgess, J.G. 2001. The symbiotic role of marine microbes on living surfaces. Hydrobiologia, 461: 37-40.
4. Barbeyron, T., L'haridon, S., Corre, E., Kloareg, B. and Potin, P. 2001. Zobellia galactanovorans gen. nov., sp. nov., a marine species of Flavobacteriaceae isolated from a red alga, and classification of three novel Zobellia species [Cytophaga] uliginosa (ZoBell & Upham 1944) Reichenbach 1989 as Zobellia uliginosa gen. nov., comb. nov. International Journal of Systematic and Evolutionary Microbiology, 51: 985-997.
5. Barrott, K.L., Rodriguez-Brito, B., Janouškovec, J., Marhaver, K.L., Smith, J.E., Keeling, P. and Rohwer, F.L. 2011. Microbial diversity associated with four functional groups of benthic reef algae and the reef-building coral Montastraea annularis. Environmental Microbiology, 13: 1192-1204.
6. Beleneva, I.A. and Zhukova, N.V. 2006. Bacterial communities of some brown and red algae from Peter the Great Bay, the Sea of Japan. Microbiology (Moscow), 75: 410-419.
7. Bode, H.B., Bethe, B., Höfs, R. and Zeeck, A. 2002. Big effects from small changes: possible ways to explore nature's chemical diversity. ChemBioChem, 3: 619-627.
8. Boyd, K.G., Adams, D.R. and Burgess, J.G. 1999. Antibacterial and repellent activities of marine bacteria associated with algal surfaces. Biofouling, 14: 227-236.
9. Burgess, J.G., Boyd, K.G., Armstrong, E., Jiang, Z., Yan, L., Berggren, M., May, U.T., Granmo, A. and Adams, D.R. 2003. The development of a marine natural product-based antifouling paint. Biofouling, 19: 197-205.
10. 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.
11. Cole, J.R., Wang, Q., Cardenas, E., Fish, J., Chai, B., Farris, R.J., Klam-Syed-Mohideen, A.S., Mccarell, D.M., Marsh, T., Garrity, G.M. and Tiedje, J.M. 2009. The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Research, 37: D141-145. (Web Server issue).
12. Collins, L.A. and Franzblau, S.G. 1997. Microplate alamar blue assay versus BACTEC 460 system for high-throughput screening of compounds against Mycobacterium tuberculosis and Mycobacterium avium. Antimicrobial Agents and Chemotherapy, 42: 1004-1009.
13. Corre, A. and Prieur, D. 1990. Density and morphology of epiphyte bacteria on the kelp Laminaria digitata. Botanica Marina, 33: 515-523.
14. Cottrell, M.T. and Kirchman, D.L. 2000. Natural assemblages of marine Proteobacteria and members of the Cytophaga-Flavobacter cluster consuming low- and high-molecular-weight dissolved organic matter. Applied and Environmental Microbiology, 66: 1692-1697.
15. Dobretsov, S., Dahms, H.U. and Qian, P.Y. 2006. Inhibition of biofouling by marine microorganisms and their metabolites. Biofouling, 22: 43-54.
16. Egan, S., Thomas, T., Holmström, C. and Kjelleberg, S. 2000. Phylogenetic relationship and antifouling activity of bacterial epiphytes from the marine alga Ulva lactuca. Environmental Microbiology, 2: 343-347.
17. Egan, S., Holmström, C. and Kjelleberg, S. 2001. Pseudoalteromonas ulvae sp. nov., a bacterium with antifouling activities isolated from the surface of a marine alga. International Journal of Systematic and Evolutionary Microbiology, 51: 1499-1504.
18. Egan, S., Thomas, T. and Kjelleberg, S. 2008. Unlocking the diversity and biotechnological potential of marine surface associated microbial communities. Current Opinion in Microbiology, 11: 219-225.
19. Engel, S., Jensen, P.R. and Fenical, W. 2002. Chemical ecology of marine microbial defense. Journal of Chemical Ecology, 28: 1971-1985.
20. Engel, S., Puglisi, M.P., Jensen, P.R. and Fenical, W. 2006. Antimicrobial activities of extracts from tropical Atlantic marine plants against marine pathogens and saprophytes. Marine Biology, 149: 991-1002.
21. Euzeby, J.P. 1997. List of bacterial names with standing in nomenclature: a folder available on the internet. International Journal of Systematic Bacteriology, 47: 590-592.
22. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution, 39: 783-791.
23. Felsenstein, J. 1989. PHYLIP-Phylogeny Interface Package (Version 3.2). Cladistics, 5: 164-166.
24. Goecke, F., Labes, A., Wiese, J. and Imhoff, J.F. 2010. Chemical interactions between marine macroalgae and bacteria. Marine Ecology Progress Series, 409: 267-300.
25. Goecke, F., Labes, A., Wiese, J. and Imhoff, J.F. 2012. Dual effect of macroalgal extracts on growth of bacteria in Western Baltic Sea. Revista de Biología Marina y Oceanografía, 47: 75-86.
26. Harder, T. 2009. "Marine epibiosis: concepts, ecological consequences and host defence". In Marine and Industrial Biofouling, Berlin: Springer. (Flemming, H.C. Murthy, P.S. Venkatesan, R. & Cooksey, K. editors), 219-231
27. Heindl, H., Wiese, J., Thiel, V. and Imhoff, J.F. 2010. Phylogenetic diversity and antimicrobial activities of bryozoan-associated bacteria isolated from Mediterranean and Baltic Sea habitats. Systematic and Applied Microbiology, 33: 94-104.
28. Hengst, M.B., Andrade, S., Gonzalez, B. and Correa, J.A. 2010. Changes in epiphytic bacterial communities of intertidal seaweeds modulated by host, temporality, and copper enrichment. Microbial Ecology, 60: 282-290.
29. Hollants, J., Leroux, O., Leliaert, F., Decleyre, H., De Clerck, O. and Willems, A. 2011. Who is in there? Exploration of endophytic bacteria within the siphonous green seaweed Bryopsis (Bryopsidales, Chlorophyta). PLOS ONE, 6: e26458
30. Holmström, C., Egan, S., Franks, A., Mccloy, S. and Kjelleberg, S. 2002. Antifouling activities expressed by marine surface associated Pseudoalteromonas species. FEMS Microbiology Ecology, 41: 47-58.
31. Hughes, C.C. and Fenical, W. 2011. Antibacterials from the sea. Chemistry-A European Journal, 16: 12512-12525.
32. Ismail-Ben Ali, A., El Bour, M., Ktari, L., Bolhuis, H., Ahmed, M., Boudabbous, A. and Stal, L.J. 2012. Jania rubens-associated bacteria: molecular identification and antimicrobial activity. Journal of Applied Phycology, 24: 525-534.
33. Ivanova, E.P., Bakunina, I.Y., Sawabe, T., Hayashi, K., Alexeeva, Y.V., Zhukova, N.V., Nicolau, D.V., Zvaygintseva, T.N. and Mikhailov, V.V. 2002. Two species of culturable bacteria associated with degradation of brown algae Fucus evanescens. Microbial Ecology, 43: 242-249.
34. Ivanova, E.P., Alexeeva, Y.A., Zhukova, N.V., Gorshkova, N.M., Buljan, V., Nicolau, D.V., Mikhailov, V.V. and Christen, R. 2004a. Bacillus algicola sp. nov., a novel filamentous organism isolated from brown alga Fucus evanescens. Systematic and Applied Microbiology, 27: 301-307.
35. Ivanova, E.P., Alexeeva, Y.V., Flavier, S., Wright, J.P., Zhukova, N.V., Gorshkova, N.M., Mikhailov, V.V., Nicolau, D.V. and Christen, R. 2004b. Formosa algae gen. nov., sp. nov., a novel member of the family Flavobacteriaceae. International Journal of Systematic and Evolutionary Microbiology, 54: 705-711.
36. Jasti, S., Sieracki, M.E., Poulton, N.J., Giewat, M.W. and Rooney-Varga, J.N. 2005. Phylogenetic diversity and specificity of bacteria closely associated with Alexandrium spp. and other phytoplankton. Applied and Environmental Microbiology, 71: 3483-3494.
37. Johansen, J.E., Nielsen, P. and Sjøholm, C. 1999. Description of Cellulophaga baltica gen. nov., sp. nov. and Cellulophaga fucicola gen. nov., sp. nov. and reclassification of [Cytophaga] lytica to Cellulophaga lytica gen. nov., comb. nov. International Journal of Systematic Bacteriology, 49: 1231-1240.
38. Kanagasabhapathy, M., Sasaki, H., Haldar, S., Yamasaki, S. and Nagata, S. 2006. Antibacterial activities of marine epibiotic bacteria isolated from brown algae of Japan. Annals of Microbiology, 56: 167-173.
39. Kanagasabhapathy, M., Sasaki, H. and Nagata, S. 2008. Phylogenetic identification of epibiotic bacteria possessing antimicrobial activities isolated from red algal species of Japan. World Journal of Microbiology and Biotechnology, 24: 2315-2321.
40. Kimura, M. 1983. The neutral theory of molecular evolution, Cambridge: Cambridge University Press.
41. Kong, M.K. and Chan, K.Y. 1979. A study on the bacterial flora isolated from marine algae. Botanica Marina, 22: 83-97.
42. Kumar, S., Tamura, K. and Nei, M. 2004. MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefings in Bioinformatics, 5: 150-163.
43. Lachnit, T., Blümel, M., Imhoff, J.F. and Wahl, M. 2009. Specific epibacterial communities on macroalgae: phylogeny matters more than habitat. Aquatic Biology, 5: 181-186.
44. Lachnit, T., Wahl, M. and Harder, T. 2010. Isolated thallus-associated compounds from the macroalga Fucus vesiculosus mediate bacterial surface colonization in the field similar to that on the natural alga. Biofouling, 26: 247-255.
45. Lachnit, T., Meske, D., Wahl, M., Harder, T. and Schmitz, R. 2011. Epibacterial community patterns on marine macroalgae are host-specific but temporally variable. Environmental Microbiology, 13: 655-665.
46. Lemos, M.L., Toranzo, A.E. and Barja, J.L. 1985. Antibiotic activity of epiphytic bacteria isolated from intertidal seaweeds. Microbial Ecology, 11: 149-163.
47. Lobban, C.S. and Harrison, P.J. 2000. Seaweed ecology and physiology, Cambridge: Cambridge University Press.
48. Longford, S.R., Tujula, N.A., Crocetti, G., Holmes, A.J., Holmström, C., Kjelleberg, S., Steinberg, P.D. and Taylor, M.W. 2007. Comparisons of diversity of bacterial communities associated with three sessile marine eukaryotes. Aquatic Microbial Ecology, 48: 217-229.
49. Muscholl-Silberhorn, A., Thiel, V. and Imhoff, J.F. 2008. Abundance and bioactivity of cultured sponge-associated bacteria from the Mediterranean Sea. Microbial Ecology, 55: 94-106.
50. Nishijima, M., Takadera, T., Imamura, N., Kasai, H., An, K.D., Adachi, K., Nagao, T., Sano, H. and Yamasato, K. 2009. Microbulbifer variabilis sp. nov. and Microbulbifer epialgicus sp. nov., isolated from Pacific marine algae, possess a rod-coccus cell cycle in association with the growth phase. International Journal of Systematic and Evolutionary Microbiology, 59: 1696-1707.
51. Nylund, G.M., Persson, F., Lindegarth, M., Cervin, G., Hermansson, M. and Pavia, H. 2010. The red alga Bonnemaisonia asparagoides regulates epiphytic bacterial abundance and community composition by chemical defence. FEMS Microbiology Ecology, 71: 84-93.
52. Palacios, L., Arahal, D.R., Reguera, B. and Marín, I. 2006. Hoeflea Alessandri sp. nov., isolated from the toxic dinoflagellate Alexandrium minutum AL1V. International Journal of Systematic and Evolutionary Microbiology, 56: 1991-1995.
53. Pankow, H. 1971. Algenflora der Ostsee. 1. Benthos, Jena: Gustav Fischer.
54. Penesyan, A., Marshall-Jones, Z., Holmström, C., Kjelleberg, S. and Egan, S. 2009. Antimicrobial activity observed among cultured epiphytic bacteria reflects their potential as source of new drugs. FEMS Microbiology Ecology, 69: 113-124.
55. Perriere, G. and Gouy, M. 1996. WWW-query: an on-line retrieval system for biological sequence banks. Biochimie, 78: 364-369.
56. Persson, F., Svensson, R., Nylund, G.M., Fredriksson, N.J., Pavia, H. and Hermansson, M. 2011. Ecological role of a secondary metabolite for a colonizing bacterial community. Biofouling, 27: 579-588.
57. Puglisi, M.P., Engel, S., Jensen, P.R. and Fenical, W. 2007. Antimicrobial activities of extracts from Indo-Pacific marine plants against marine pathogens and saprophytes. Marine Biology, 150: 531-540.
58. Rao, D., Webb, J.S., Holmström, C., Case, R., Low, A., Steinberg, P. and Kjelleberg, S. 2007. Low densities of epiphytic bacteria from the marine alga Ulva australis inhibits settlement of fouling organisms. Applied and Environmental Microbiology, 73: 7844-7852.
59. Romanenko, L.A., Zhukova, N.V., Lysenko, A.M., Mikhailov, V.V. and Stackebrandt, E. 2003. Assignment of "Alteromonas marinoglutinosa" NCIMB 1770 to Pseudoalteromonas mariniglutinosa sp. nov., nom. rev., comb. nov. International Journal of Systematic and Evolutionary Microbiology, 53: 1105-1109.
60. Saha, M., Rempt, M., Grosser, K., Pohnert, G. and Weinberger, F. 2011. Surface-associated fucoxanthin mediates settlement of bacterial epiphytes on the rockweed Fucus vesiculosus. Biofouling, 27: 423-433.
61. Saitou, N. and Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4: 406-425.
62. Sawabe, T., Makino, H., Tatsumi, M., Nakano, K., Tajima, K., Iqbal, M.M., Yumoto, I., Ezura, Y. and Christen, R. 1998. Pseudoalteromonas bacteriolytica sp. nov., a marine bacterium that is the causative agent of red spot disease of Laminaria japonica. International Journal of Systematic Bacteriology, 48: 769-774.
63. T and five strains isolated from spot wounded fronds of Laminaria japonica to Pseudoalteromonas elyakovii comb. nov. and the extended description of the species. International Journal of Systematic Bacteriology, 50: 265-271.
64. Schneemann, I., Nagel, K., Kajahn, I., Labes, A., Wiese, J. and Imhoff, J.F. 2010. Comprehensive investigation of marine Actinobacteria associated with the sponge Halichondria panacea. Applied and Environmental Microbiology, 76: 3702-3714.
65. Shiba, T.O. and Taga, N. 1980. Heterotrophic bacteria attached to seaweeds. Journal of Experimental Marine Biology and Ecology, 47: 251-258.
66. Skovhus, T.L., Holmström, C., Kjelleberg, S. and Dahllöf, I. 2007. Molecular investigation of the distribution, abundance and diversity of the genus Pseudoalteromonas in marine samples. FEMS Microbiology Ecology, 61: 348-361.
67. Sneed, J.M. and Pohnert, G. 2011. The green alga Dictyosphaeria ocellata and its organic extracts alter natural bacterial biofilms communities. Biofouling, 27: 347-356.
68. Staufenberger, T., Thiel, V., Wiese, J. and Imhoff, J.F. 2008. Phylogenetic analysis of bacteria associated with Laminaria saccharina. FEMS Microbiology Ecology, 64: 65-77.
69. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 24: 4876-4882.
70. Todorova, S. and Kozhuharova, L. 2010. Characteristics and antimicrobial activity of Bacillus subtilis strains isolated from soil. World Journal of Microbiology and Biotechnology, 26: 1207-1216.
71. Tujula, N.A., Crocetti, G.R., Burke, C., Thomas, T., Holmström, C. and Kjelleberg, S. 2010. Variability and abundance of the epiphytic bacterial community associated with a green marine Ulvacean alga. ISME Journal, 4: 301-311.
72. Vairappan, C.S., Anangdan, S.P., Tan, K.L. and Matsunaga, S. 2010. Role of secondary metabolites as defense chemicals against ice-ice disease bacteria in biofouler at carrageenophyte farms. Journal of Applied Phycology, 22: 305-311.
73. Villarreal-Gómez, L.J., Soria-Mercado, I.E., Guerra-Rivas, G. and Ayala-Sánchez, N.E. 2010. Antibacterial and anticancer activityof seaweeds and bacteria associated with their surface. Revista de Biología Marina y Oceanografía, 45: 267-275.
74. Vynne, N.J., Mansson, M., Nielsen, K.F. and Gram, L. 2011. Bioactivity, chemical profiling, and 16S rRNA-based phylogeny of Pseudoalteromonas strains collected on a global research cruise. Marine Biotechnology, 13: 1062-1073.
75. Wahl, M., Shahnaz, L., Dobretsov, S., Saha, M., Symanowski, F., David, K., Lachnit, T., Vasel, M. and Weinberger, F. 2010. Ecology of antifouling resistance in the bladder wrack Fucus vesiculosus: patterns of microfouling and antimicrobial protection. Marine Ecology Progress Series, 411: 33-48.
76. Wiese, J., Thiel, V., Nagel, K., Staufenberger, T. and Imhoff, J.F. 2009. Diversity of antibiotic active bacteria associated with the brown alga Laminaria saccharina from the Baltic Sea. Marine Biotechnology, 11: 287-300.
77. Zheng, L., Han, X., Chen, H., Lin, W. and Yan, X. 2005. Marinebacteria associated with marine macroorganisms: the potential antimicrobial resources. Annals of Microbiology, 55: 119-124.