A new method for removing microflora from macroalgal surfaces: An important step for natural product discovery

Botanica Marina

Volumn 54, Issue 5, 2011, Pages 457-469

  Kientz, Betty ^a   Thabard, Marie ^a   Cragg, Simon M ^a   Pope, Josephine ^a   Hellio, Claire ^a  

^a UNIVERSITY OF PORTSMOUTH   (United Kingdom)

Author keywords

epibionts; macroalgae; microflora; natural product discovery; surface disinfection

Indexed keywords

BIOACTIVITY; BIOLOGICAL PRODUCTION; BIOTECHNOLOGY; EPIBIONT; ETHANOL; MACROALGA; MOISTURE CONTENT; PLANT EXTRACT; SCANNING ELECTRON MICROSCOPY; SECONDARY METABOLITE;

ALGAE; CHONDRUS; CHONDRUS CRISPUS; FUCUS; FUCUS SERRATUS; LACTUCA; MELALEUCA ALTERNIFOLIA; PALMARIA PALMATA; SACCHARINA LATISSIMA; ULVA; ULVA LACTUCA;

EID: 80053621734     PISSN: 00068055     EISSN: 14374323     Source Type: Journal    
DOI: 10.1515/BOT.2011.053     Document Type: Article

References (94)

1. Aguirre-Lipperheide, M. and L.V. Evans. 1993. A sterilization protocol for the Dictyotales (Phaeophyceae) 1. J. Phycol. 29: 243-251.
2. Almeida, M.G., M. Humanes, R. Melo, J.A. Silva, J. da Silva and R. Wever. 2000. Purification and characterisation of vanadium haloperoxidases from the brown alga Pelvetia canaliculata. Phytochemistry 54: 5-11. (Pubitemid 30337399)
3. Anand, T.P., A.W. Bhata, Y.S. Shoucheb, U. Royb, J. Siddharthb and P.S. Siddhartha. 2006. Antimicrobial activity of marine bacteria associated with sponges from the waters off the coast of South East India. Microbiol. Res. 161: 252-262. (Pubitemid 43831616)
4. Armstrong, E., L.M. Yan, K.G. Boyd, P.C. Wright and J.G. Burgess. 2001. The symbiotic role of marine microbes on living surfaces. Hydrobiologia 461: 37-40. (Pubitemid 34067986)
5. Atlas, R.M. 2004. Handbook of microbiological media. CRC Press, London.
6. Atlas, R.M. and L.C. Parks. 1993. Handbook of microbiological culture media. CRC Press, London.
7. Baker, J.T. 1984. Seaweeds in pharmaceutical studies and applications. Hydrobiologia 116-117: 29-40.
8. Baweja, P., D. Sahoo, P. Garćá-Jiménez and R.R. Robaina. 2009. Seaweed tissue culture as applied to biotechnology: problems, achievements and prospects. Phycol. Res. 57: 45-58.
9. Bernan, V.S., M. Greenstein and W.M. Maiese. 1997. Marine microorganisms as a source of new natural products. Adv. Appl. Microbiol. 43: 57-90. (Pubitemid 27186672)
10. Blunt, J.W., B.R. Copp, W.P. Hu, M.H.G. Munro, P.T. Northcote and M.R. Prinsep. 2009. Marine natural products. Nat. Prod. Rep. 26: 170-244.
11. Boyd, K.G., D.R. Adams and J.G. Burgess. 1999. Antibacterial and repellent activities of marine bacteria associated with algal surfaces. Biofouling 14: 227-236. (Pubitemid 30049178)
12. Bradley, P.M., D.P. Cheney and N. Saga. 1988. One step antibiotic disk method for obtaining axenic cultures of multicellular marine algae. Plant Cell Tiss. Org. Cult. 12: 55-60.
13. Callow, M.E., L.V. Evans, G.P. Bolwell and J.A. Callow. 1978. Fertilization in brown-algae. 1. SEM and other observations on Fucus serratus. J. Cell Sci. 32: 45-54. (Pubitemid 8392498)
14. Carlsen, B.P., G. Johnsen, J. Berge and P. Kuklinski. 2007. Biodiversity patterns of macro-epifauna on different lamina parts of Laminaria digitata and Saccharina latissima collected during spring and summer 2004 in Kongsfjorden, Svalbard. Polar Biol. 30: 939-943. (Pubitemid 46742581)
15. Characklis, W.G. and J.D. Bryers. 1981. Bioengineering report. Fouling biofilm development: a process analysis. Biotechnol. Bioeng. 23: 1923-1960.
16. Choi, J.S., J. Cho, L. Jin, H. Jin and Y. Hong. 2002. Procedures for the axenic isolation of conchocelis and monospores from the red seaweed Porphyra yezoensis. J. Appl. Phycol. 14: 115-121. (Pubitemid 34536166)
17. Clare, A.S. 1996. Natural product antifoulants: status and potential. Biofouling 9: 211-229. (Pubitemid 126565645)
18. Clare, A.S. 1998. Towards nontoxic antifouling. J. Mar. Biotechnol. 6: 3-6.
19. Colwell, R.R. and D.J. Grimes. 2000. Nonculturable microorganisms in the environment. American Society for Microbiology/ASM Press, Washington, DC.
20. Costerton, J.W. 1999. Introduction to biofilm. Int. J. Antimicrob. Agents 11: 217-221. (Pubitemid 29231963)
21. Davey, M.E. and G.A. O'Toole. 2000. Microbial biofilms: from ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 64: 847-867. (Pubitemid 32475933)
22. De La Maza, L.M., M.T. Pezzlo, J.T. Shigei and E. Peterson. 2004. Color atlas of medical bacteriology. American Society for Microbiology/ASM Press, Washington, DC.
23. De Nys, R., S.A. Dworjanyn and P.D. Steinberg. 1998. A new method for determining surface concentrations of marine natural products on seaweeds. Mar. Ecol. Prog. Ser. 162: 79-87. (Pubitemid 28140041)
24. Debashish, G., S. Malay, S. Barindra and M. Joydeep. 2005. Marine enzymes. Mar. Biotechnol. 96: 189-218. (Pubitemid 44641521)
25. Debeer, D., R. Srinivasan and P.S. Stewart. 1994. Direct measurement of chlorine penetration into biofilms during disinfection. Appl. Environ. Microbiol. 60: 4339-4344. (Pubitemid 24370800)
26. Decho, A.W. 2000. Microbial biofilms in intertidal systems: an overview. Cont. Shelf Res. 20: 1257-1273. (Pubitemid 30647422)
27. Donlan, R.M. 2002. Biofilms: microbial life on surfaces. Emerg. Infect. Dis. 8: 881-890. (Pubitemid 35000803)
28. Donnell, G.E.M. 2007. Antisepsis, disinfection and sterilization: types, action, and resistance. ASM Press, Washington, DC. pp. 361.
29. Faulkner, D.J. 2001. Marine natural products. Nat. Prod. Rep. 18: 1-49. (Pubitemid 32160982)
30. Faulkner, J. 1993. Academic chemistry and the discovery of bioactive marine natural products. In: (D.H. Attaway and O.R. Zaborsky, eds) Marine biotechnology: pharmaceutical and bioactive natural products. Plenum Press, New York. pp. 459-470.
31. Fries, L. 1980. Axenic tissue cultures from the sporophytes of Laminaria digitata and Laminaria hyperborea (Phaeophyta). J. Phycol. 16: 475-477.
32. Fu, T., G. Singh and W.R. Curtis (eds). 1999. Plant cell and tissue culture for the production of food ingredients: an introduction. Division of Agricultural and Food Chemistry of the American Chemical Society. Kluwer Academic/Plenum Publishers, New York. pp. 296.
33. Fusetani, N. 2004. Biofouling and antifouling. Nat. Prod. Rep. 21: 94-104. (Pubitemid 38260875)
34. Garcia-Jiménez, P., M. Rodrigo and R.R. Robaina. 1998. Influence of plant growth regulators, polyamines and glycerol interaction on growth and morphogenesis of carposporelings of Grateloupia cultured in vitro. J. Appl. Phycol. 10: 95-100. (Pubitemid 28326469)
35. Gledhill, M., M.T. Brown, M. Nimmo, R. Moate and S.J. Hill. 1998. Comparison of techniques for the removal of particulate material from seaweed tissue. Mar. Environ. Res. 45: 295-307. (Pubitemid 28336359)
36. Guillard, R.R.L. and J.H. Ryther. 1962. Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea Cleve. Can. J. Microbiol. 8: 229-239.
37. Gusev, M.V., A.H. Tambiev, N.N. Kirikova, R.R. Aslanyan and N.N. Shelyastina. 1984. Obtaining of axenic explants from marine algae thallus. Izv. Acad. Nauk. USSR ser. Biol. 5: 716-721 (in Russian).
38. Gusev, M.V., A.H. Tambiev, N.N. Kirikovan, N.N. Shelyastina and R.R. Aslanyan. 1987. Callus formation in seven species of agarophyte marine algae. Mar. Biol. 95: 593-597.
39. Haglund, A.L., E. Törnblom, B. Boström and L. Tranvik. 2002. Large differences in the fraction of active bacteria in plankton, sediments, and biofilm. Microb. Ecol. 43: 232-241. (Pubitemid 36941352)
40. Hall-Stoodley, L., J.W. Costerton and P. Stoodley. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat. Rev. Microbiol. 2: 95-108. (Pubitemid 39490064)
41. Harder, T. 2009. Marine epibiosis: concepts, ecological consequences and host defence. In: (H.C. Flemming, P.S. Murthy, R. Venkatesan and K.E. Cooksey, eds) Marine and industrial biofouling (Springer Series on Biofilms). Springer-Verlag, Berlin/Heidelberg. pp. 219-232.
42. Harrison, P.J. and J.A. Berges. 2005. Marine culture media. In: (R.A. Andersen, ed.) Algal culturing techniques. Elsevier Academic Press, London. pp. 21-34.
43. Haygood, M.G., E.W. Schmidt, S.K. Davidson and D.J. Faulkner. 1999. Microbial symbionts of marine invertebrates: opportunities for microbial biotechnology. J. Mol. Microbiol. Biotechnol. 1: 33-43. (Pubitemid 129491922)
44. Hellio, C., D. De La Broise, L. Dufosse, Y. Le Gal and N. Bourgougnon. 2001. Inhibition of marine bacteria by extracts of macroalgae: potential use for environmentally friendly antifouling paints. Mar. Environ. Res. 52: 231-247. (Pubitemid 32780975)
45. Hellio, C., J.P. Maréchal, B. Da Gama, R. Pereira and A.S. Clare. 2009. Natural marine products with antifouling activities. In: (C. Hellio and D. Yebra, eds) Advances in marine antifouling coatings and technologies. Woodshead Publishing, Cambridge. pp. 572-622.
46. Huang, L.N., H. De Wever and L. Diels. 2008. Diverse and distinct bacterial communities induced biofilm fouling in membrane bioreactors operated under different conditions. Environ. Sci. Technol. 42: 8360-8366.
47. Jensen, P.R. and W. Fenical. 1996. Marine bacterial diversity as a resource for novel microbial products. J. Ind. Microbiol. Biotechnol. 17: 346-351.
48. Jones, E.B.G. 2008. Bioactive compounds in marine organisms. Bot. Mar. 51: 161-162.
49. Jordan, P., B. Kloareg and H. Vilter. 1991. Detection of vanadatedependent bromoxidases in protoplasts from brown-algae Laminaria digitata and Laminaria saccharina. J. Plant Physiol. 137: 520-524.
50. Kawashima, Y. and H. Tokuda. 1993. Regeneration from callus of Undaria pinnatifida (Harvey) Suringar (Laminariales, Phaeophyta). Hydrobiologia 260-261: 385-389.
51. Kelecom, A. 2002. Secondary metabolites from marine microorganisms. An. Acad. Bras. Cienc. 74: 151-170. (Pubitemid 135695062)
52. Kohlmeyer, J. and B. Volkmann-Kohlmeyer. 2003. Marine ascomycetes from algae and animal hosts. Bot. Mar. 46: 285-306. (Pubitemid 36619019)
53. Lachnit, T., M. Blümel, J.F. Imhoff and M. Wahl. 2009. Specific epibacterial communities on macroalgae: phylogeny matters more than habitat. Aquat. Biol. 5: 181-186.
54. Lawlor, H.J., M.A. Borowitzka and J.A. McComb. 1991. A rapid and inexpensive method for surface sterilisation of Ecklonia radiata (Phaeophyta) for tissue culture. Bot. Mar. 34: 261-264.
55. Leblanc, C., C. Colin, A. Cosse, L. Delage, S. La Barre, P. Morin, B. Fiévet, C. Voiseux, Y. Ambroise, E. Verhaeghe, D. Amouroux, O. Donard, E. Tessier and P. Potin. 2006. Iodine transfers in the coastal marine environment: the key role of brown algae and of their vanadium-dependent haloperoxidases. Biochimie 88: 1773-1785. (Pubitemid 44781275)
56. Loaec, M., R. Olier and J. Guezennec. 1997. Uptake of lead, cadmium and zinc by a novel bacterial exopolysaccharide. Water Res. 31: 1171-1179. (Pubitemid 27192555)
57. Lobban, C.S. and P.J. Harrison. 1994. Seaweed ecology and physiology. Cambridge University Press, Cambridge. pp. 366.
58. Lüning, K. 1990. Seaweeds: their environment, biogeography and ecophysiology. John Wiley & Sons Press, New York. pp. 527.
59. Mack, D., W. Fischer, A. Krokotsch, K. Leopold, R. Hartmann, H. Egge and R. Laufs. 1996. The intercellular adhesin involved in biofilm accumulation of Staphylococcus epidermidis is a linear beta-1,6-linked glucosaminoglycan: purification and structural analysis. J. Bacteriol. 178: 175-183. (Pubitemid 26006081)
60. Mayer, C., R. Moritz, C. Kirschner, W. Borchard, R. Maibaum, J. Wingender and H.C. Flemming. 1999. The role of intermolecular interactions: studies on model systems for bacterial biofilms. Int. J. Biol. Macromol. 26: 3-16. (Pubitemid 29457825)
61. Mayer, A.M.S., A.D. Rodríguez, R.G.S. Berlinck and M.T. Hamannd. 2009. Marine pharmacology in 2005-6: marine compounds with anthelmintic, antibacterial, anticoagulant, antifungal, anti-inflammatory, antimalarial, antiprotozoal, antituberculosis, and antiviral activities; affecting the cardiovascular, immune and nervous systems, and other miscellaneous mechanisms of action. Biochim. Biophys. Acta 1790: 283-308.
62. McCandless, E.L. 1981. Polysaccharides of seaweeds. In: (C.S. Lobban and M.J. Wynne, eds) The biology of seaweeds. Botanical monograph. Vol. 17. University of California Press, Berkeley/Los Angeles, CA. pp. 559-588.
63. Mérour, J.Y. 2004. La mer, source de molécules bioactives. Sciences 3: 15-22.
64. Molinski, T.F., D.S. Dalisay, S.L. Lievens and J.P. Saludes. 2009. Drug development from marine natural products. Nat. Rev. Drug Discov. 8: 69-85.
65. Nye, K.J., D. Fallon, D. Frodsham, B. Gee, C. Graham, S. Howe, S. Messer, T. Turner and R.E. Warren. 2002. An evaluation of the performance of XLD, DCA, MLCB, and ABC agars as direct plating media for the isolation of Salmonella enterica from faeces. J. Clin. Pathol. 55: 286-288. (Pubitemid 34293396)
66. Okami, Y. 1986. Marine microorganisms as a source of bioactive agents. Microb. Ecol. 12: 65-78. (Pubitemid 16092730)
67. Paul, V.J. and M.P. Puglisi. 2004. Chemical mediation of interactions among marine organisms. Nat. Prod. Rep. 21: 189-209. (Pubitemid 38260881)
68. Prieur, D., F. Gaill and S. Corre. 1993. Complex epibiotic bacterial communities on marine organisms: fouling or interactions? In: (Guerrero, R. & C. Pedrós-Alió eds), Trends in Microbial Ecology. Spanish Society for Microbiology, Barcelona, pp. 207-212.
69. Proksch, P., R. Edrada and R. Ebel. 2002. Drugs from the seas - current status and microbiological implications. Appl. Microbiol. Biotechnol. 59: 125-134. (Pubitemid 34756951)
70. Qian, P.Y., S.C.K. Lau, H.U. Dahms, S. Dobretsov and T. Harder. 2007. Marine biofilms as mediators of colonization by marine macroorganisms: implications for antifouling and aquaculture. Mar. Biotechnol. 9: 399-410. (Pubitemid 47492126)
71. Ralston, E. and G. Swain. 2009. Bioinspiration - the solution for biofouling control? Bioinspir. Biomimet. 4: 1-9.
72. Reddy, C.R.K., B. Jha, Y. Fujita and M. Ohno. 2008. Seaweed micropropagation techniques and their potentials: an overview. J. Appl. Phycol. 20: 609-617.
73. Renn, D.W. 1990. Seaweeds and biotechnology - inseparable companions. Hydrobiologia 204-205: 7-13.
74. Rorrer, G.L. and D.P. Cheney. 2004. Bioprocess engineering of cell and tissue cultures for marine seaweeds. Aquacult. Eng. 32: 11-41. (Pubitemid 39444447)
75. Rosell, K.G. and L.M. Srivastava. 1987. Fatty acids as antimicrobial substances in brown-algae. Hydrobiologia 151: 471-475.
76. Scardino, A.J., D. Hudleston, Z. Peng, N.A. Paul and R. de Nys. 2009. Biomimetic characterisation of key surface parameters for the development of fouling resistant materials. Biofouling 25: 83-93.
77. Schulz, B., S. Guske, U. Dammann and C. Boyle. 1998. Endophyte-host interactions. II. Defining symbiosis of the endophyte-host interaction. Symbiosis 25: 213-227. (Pubitemid 28382750)
78. Schulz, B., S. Draeger, T.E. de la Cruz, J. Rheinheimer, K. Siems, S. Loesgen, J. Bitzer, O. Schloerke, A. Zeeck, I. Kock, H. Hussain, J.Q. Dai and K. Krohn. 2008. Screening strategies for obtaining novel, biologically active, fungal secondary metabolites from marine habitats. Bot. Mar. 51: 219-234.
79. Sieburth, J.M.N. 1969. Studies on algal substances in the sea. III. The production of extracellular organic matter by littoral marine algae. J. Exp. Mar. Biol. Ecol. 3: 290-309.
80. Sponga, F., L. Cavaletti, A. Lazzarini, A. Borghi, I. Ciciliato, D. Losi and F. Marinelli. 1999. Biodiversity and potentials of marine-derived microorganisms. J. Biotechnol. 70: 65-69. (Pubitemid 29299261)
81. Steinberg, P.D. and R. De Nys. 2002. Chemical mediation of colonization of seaweed surfaces. J. Phycol. 38: 621-629. (Pubitemid 34979228)
82. Steinberg, P.D., R. De Nys and S. Kjelleberg. 2002. Chemical cues for surface colonization. J. Chem. Ecol. 28: 1935-1951. (Pubitemid 35365098)
83. Stoodley, P., K. Sauer, D.G. Davies and J.W. Costerton. 2002. Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 56: 187-209. (Pubitemid 35217453)
84. Sutherland, I.W. 2001. Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 147: 3-9. (Pubitemid 32094304)
85. Vilter, H., K.W. Glombitza and A. Grawe. 1983. Peroxidases from Phaeophyceae. 1. Extraction and detection of the peroxidases. Bot. Mar. 26: 331-339.
86. Wahl, M. 1989. Marine epibiosis. I. Fouling and antifouling: some basic aspects. Mar. Ecol. Prog. Ser. 58: 175-189.
87. Wahl, M. 2008. Ecological lever and interface ecology: epibiosis modulates the interactions between host and environment. Biofouling 24: 427-438.
88. Wahl, M., K. Kroeger and M. Lenz. 1998. Non-toxic protection against epibiosis. Biofouling 12: 1-3.
89. Wilson, T.A., S. Graham, A. Miles, A. Knox, R. Parker, M.T. Macrae, A.D. Meynell, G.G. Meynell, W. Elinor. 1964. Topley and Wilson's principles of bacteriology and immunity. Edward Arnold, London. pp. 1964.
90. Xuewu, L. and B. Kloareg. 1992. Explant axenisation for tissue culture in marine macroalgae. Chin. J. Oceanol. Limnol. 10: 268-275.
91. Xue-wu, L. and M.E. Gordon. 1987. Tissue and cell culture of New Zealand Pterocladia and Porphyra species. Hydrobiologia 151-152: 147-154.
92. Zheng, L., X.T. Han, H.M. Chen, W. Lin and X.J. Yan. 2005. Marine bacteria associated with marine macroorganisms: the potential antimicrobial resources. Ann. Microbiol. 55: 119-124. (Pubitemid 40885998)
93. Zobell, C.E. 1941. Studies on marine bacteria. I. The cultural requirements of heterotrophic aerobes. J. Mar. Res. 4: 42-75.
94. Zuccaro, A., C.L. Schoch, J.W. Spatafora, J. Kohlmeyer, S. Draeger and J.I. Mitchel. 2007. Detection and identification of fungi intimately associated with the brown seaweed Fucus serratus. Appl. Environ. Microbiol. 74: 931-941.