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Antidiatom and antibacterial activity of epiphytic bacteria isolated from Ulva lactuca in tropical waters

  • V. KumarEmail author
  • D. Rao
  • T. Thomas
  • S. Kjelleberg
  • S. Egan
Original Paper

Abstract

Bacteria and diatoms are primary colonizers of marine surfaces and hence play a crucial role in the attachment and subsequent growth of macroorganisms. It has been suggested that the temperate green alga Ulva lactuca relies on the defence provided by the epiphytic bacterial community to regulate surface fouling of colonising organisms. In this study, ten resident bacterial isolates from tropical U. lactuca were tested for their antibacterial and antidiatom properties that may regulate surface colonization on the algae. Sixty percent of the epiphytic isolates expressed antibacterial properties against other resident bacteria and 80% had antidiatom activity against the pennate diatom, Cylindrotheca fusiformis. Isolates of the Pseudoalteromonas genus showed both- antibacterial and antidiatom activities, while members of the genus Bacillus, Vibrio and Shewanella mostly possessed antidiatom activity. Our results show that a high proportion of bacterial isolates from tropical U. lactuca, like that of their temperate counterparts contain antibiotic properties that might impact on the bacterial community composition and prevent fouling by diatoms.

Keywords

Antibacterial Antidiatom Tropical waters Ulva Epiphytic bacteria 

Notes

Acknowledgments

We thank the Faculty of Science, Technology and Environment, University of the South Pacific and the Centre for Marine Bio-Innovation, University of New South Wales, for funding the study.

References

  1. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410Google Scholar
  2. Bhattarai H, Lee Y, Cho K, Lee H, Shin H (2006) The study of antagonistic interactions among pelagic bacteria: a promising way to coin environmental friendly antifouling compounds. Hydrobiologia 568:417–423CrossRefGoogle Scholar
  3. Bhattarai H, Granti V, Paudel B, Lee Y, Lee H, Hong Y, Shin H (2007) Isolation of antifouling compounds from the marine bacterium, Shewanela oneidensis SCH0402. World J Microbiol Biotechnol 23:243–249CrossRefGoogle Scholar
  4. Bowman J (2007) Bioactive compound synthetic capacity and ecological significance of marine bacterial genus Pseudoalteromonas. Mar Drugs 5:220–241Google Scholar
  5. Braithwaite RA, McEvoy LA (2004) Marine biofouling on fish farms and its remediation. In: Southward AJ, Tyler PA, Young CM, Fulman A (eds) Advances in marine biology. Academic Press, London, pp 215–252Google Scholar
  6. Campàs C, Dalmau M, Montaner B, Barragán M, Bellosillo B, Colomer D, Pons G, Pérez-Tomás R, Gil J (2003) Prodigiosin induces apoptosis of B and T cells from B-cell chronic lymphocytic leukemia. Leukemia 17:746–750CrossRefGoogle Scholar
  7. Chan AT, Andersen RJ, Blanc MJ, Harrison PJ (1980) Algal plating as a tool for investigating allelopathy among marine microalgae. Mar Biol 59:7–13CrossRefGoogle Scholar
  8. Coley PD (1986) Costs and benefits of defence by tannins in a neotropical tree. Oecologia 70:238–241CrossRefGoogle Scholar
  9. Dobretsov S, Qian PY (2002) Effect of bacteria associated with the green alga Ulva reticulata on marine micro- and macrofouling. Biofouling 18:217–228CrossRefGoogle Scholar
  10. Dobretsov S, Dahms H-U, Qian P-Y (2006) Inhibition of biofouling by marine microorganisms and their metabolites. Biofouling 22:43–54CrossRefGoogle Scholar
  11. Egan S, Thomas T, Holmström C, Kjelleberg S (2000) Phylogenetic relationship and antifouling activity of bacterial epiphytes from the marine alga Ulva lactuca. Environ Microbiol 2:343–347CrossRefGoogle Scholar
  12. Egan S, Holmstrom C, Kjelleberg S (2001) Pseudoalteromonas ulvae sp. nov., a bacterium with antifouling activities isolated from the surface of a marine alga. Int J Syst Evol Microbiol 51:1499–1504Google Scholar
  13. Egan S, Thomas T, Kjelleberg S (2008) Unlocking the diversity and biotechnological potential of marine surface associated microbial communities. Curr Opin Microbiol 11:219–225CrossRefGoogle Scholar
  14. Evans SM, Leksono T, McKinnell PD (1995) Tributyltin pollution: a diminishing problem following legislation limiting the use of TBT-based antifouling paints. Mar Poll Bull 30:14–21CrossRefGoogle Scholar
  15. Ferrari BC, Winsley T, Gillings M, Binnerup S (2008) Cultivating previously uncultured soil bacteria using a soil substrate membrane system. Nat Protocols 3:1261–1269CrossRefGoogle Scholar
  16. Fusetani N (2004) Biofouling and antifouling. Nat Prod Rep 21:94–104CrossRefGoogle Scholar
  17. Gerber N, Gauthier M (1979) New prodigiosin-like pigment from Alteromonas rubra. Appl Environ Microbiol 37:1176–1179Google Scholar
  18. Gontang E, Fenical W, Jensen P (2007) Phylogenetic diversity of Gram-Positive bacteria cultured from marine sediments. Appl Environ Microbiol 73:3272–3282CrossRefGoogle Scholar
  19. Harder T, Dobretsov S, Qian P-Y (2004) Waterborne polar macromolecules act as algal antifoulants in the seaweed Ulva reticulata. Mar Ecol Prog Ser 274:133–141CrossRefGoogle Scholar
  20. Holmström C, Egan S, Franks A, McCloy S, Kjelleberg S (2002) Antifouling activities expressed by marine surface associated Pseudoalteromonas species. FEMS Microbiol Ecol 41:47–58Google Scholar
  21. Hugenholtz P (2002) Exploring prokaryotic diversity in the genomic era. Genome Biology 3: reviews 0003.0001Google Scholar
  22. Huggett M, Williamson J, Nys R, Kjelleberg S, Steinberg P (2006) Larval settlement of the common Australian sea urchin Heliocidairs erythrogramma in response to bacteria from the surface of coralline algae. Oceologia 149:604–619CrossRefGoogle Scholar
  23. Kanagasabhapathy M, Sasaki H, Nagata S (2008) Phylogenetic identification of epibiotic bacteria possessing antimicrobial activities isolated from red algal species of Japan. World J Microbiol Biotechnol 24:2315–2321CrossRefGoogle Scholar
  24. Kang YH, Kim JD, Kim BH, Kong DS, Han MS (2005) Isolation and characterization of a bio-agent antagonistic to diatom, Stephanodiscus hantzschii. J Appl Microbiol 98:1030–1038CrossRefGoogle Scholar
  25. Kawauchi K, Shibutani K, Yagisawa H, Kamata H, Nakatsuji S, Anzai H, Yokoyama Y, Ikegami Y, Moriyama Y, Hirata H (1997) A possible immunosuppressant, cycloprodigiosin hydrochloride, obtained from Pseudoalteromonas denitrificans. Biochem Biophys Res Comm 237:543–547CrossRefGoogle Scholar
  26. Keats DW, Knight MA, Pueschel CM (1997) Antifouling effects of epithelial shedding in three crustose corralling algae (Rhodophyta, Coralines) on a coral reef. J Exp Mar Biol Ecol 213:281–293CrossRefGoogle Scholar
  27. Kim H, Hayashi M, Shibata Y, Wataya Y, Mitamura T, Horii T, Kawauchi K, Hirata H, Tsuboi S, Moriyama Y (1999) Cycloprodigiosin hydrochloride obtained from Pseudoalteromonas denitrificans is a potent antimalarial agent. Biol Pharm Bull 22:532–534Google Scholar
  28. Longford SR, Tujula NA, Crocetti GR, Holmes AJ, Holmstr√∂m C, Kjelleberg S, Steinberg PD, Taylor MW (2007) Comparisons of diversity of bacterial communities associated with three sessile marine eukaryotes. Aquatic Microbial Ecol 48:217–229CrossRefGoogle Scholar
  29. Maata M, Koshy K (2001) A study on tributyltin contamination of marine sediments in the major ports of Fiji. South Pac J Nat Sci 19:1–4Google Scholar
  30. Magae J, Miller M, Nagai K, Shearer G (1996) Effect of metacycloprodigiosin, an inhibitor of killer T cells on murine skill and heart transplants. J Antibiot 48:86–90Google Scholar
  31. Moss B (1982) The control of epiphytes by Halidrys siliquosa (L.) Lynbg. (Phaeophyta, Cystoseiraceae). Phycologia 21:185–191CrossRefGoogle Scholar
  32. Nylund GM, Pavia H (2005) Chemical versus mechanical inhibition of fouling in the red alga Dilsea carnosa. Mar Ecol Prog Ser 299:111–121CrossRefGoogle Scholar
  33. Nylund GM, Persson F, Lindegarth M, Cervin G, Hermansson M, Pavia H (2010) The red alga Bonnemaisonia asparagoides regulates epiphytic bacterial abundance and community composition by chemical defence. FEMS Microbiol Ecol 71:84–93CrossRefGoogle Scholar
  34. Ortega-Morales B, Chan-Bacab M, Miranda-Tello E, Fardeau M, Carrero J, Stein T (2008) Antifouling activity of sessile bacilli derived from marine surfaces. J Ind Microbiol Biotechnol 35:9–15CrossRefGoogle Scholar
  35. Penesyan A, Marshall-Jones Z, Holmstrom C, Kjelleberg S, Egan S (2009) Antimicrobial activity observed among cultured marine epiphytic bacteria reflects their potential as a source of new drugs. FEMS Microbiol Ecol 69:113–124CrossRefGoogle Scholar
  36. Penesyan A, Kjelleberg S, Egan S (2010) Development of novel drugs from marine surface associated microorganisms. Mar Drugs 8:438–459CrossRefGoogle Scholar
  37. Perez-Tomas R, Montaner B, Llagostera R, Soto-Cerrato V (2003) The prodigiosins, proapoptotic drugs with anticancer properties. Biochem Pharmacol 66:1447–1452CrossRefGoogle Scholar
  38. Qian P-Y, Xu Y, Fusetani N (2010) Natural products as antifouling compounds: recent progress and future perspectives. Biofouling 26:223–234CrossRefGoogle Scholar
  39. Rao D, Webb JS, Kjelleberg S (2005) Competitive interactions in mixed-species biofilms containing the marine bacterium Pseudoalteromonas tunicata. Appl Environ Microbiol 71:1729–1736CrossRefGoogle Scholar
  40. Rappe MS, Giovannoni SJ (2003) The uncultured microbial majority. Annu Rev Microbiol 57:369–394CrossRefGoogle Scholar
  41. Silva-Aciares F, Riquelme C (2008) Inhibition of attachment of some fouling diatoms and settlement of Ulva lactuca zoospores by film-forming bacterium and their extracellular products isolated from biofouled substrata in Northern Chile. Elect J Biotechnol 11:60–70Google Scholar
  42. Skovhus TL, Holmström C, Kjelleberg S, Dahllöf I (2007) Molecular investigation of the distribution, abundance and diversity of the genus Pseudoalteromonas in marine samples. FEMS Microbiol Ecol 61:348–361CrossRefGoogle Scholar
  43. Tillett D, Neilan BA (2000) Xanthogenate nucleic acid isolation from cultured and environmental cyanobacteria. J Phycol 36:251–258CrossRefGoogle Scholar
  44. Tujula NA, Crocetti GR, Burke C, Thomas T, Holmstrom C, Kjelleberg S (2009) Variability and abundance of the epiphytic bacterial community associated with a green marine Ulvacean alga. ISME J 4:301–311CrossRefGoogle Scholar
  45. Vartoukian SR, Palmer RM, Wade WG (2010) Strategies for culture of ‘unculturable’ bacteria. FEMS Microbiol Lett 309:1–7Google Scholar
  46. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267CrossRefGoogle Scholar
  47. Yebra DM, Kiil Sr, Dam-Johansen K (2004) Antifouling technology–past, present and future steps towards efficient and environmentally friendly antifouling coatings. Prog Organic Coat 50:75–104CrossRefGoogle Scholar
  48. Zengler K, Toledo G, Rappe M, Elkins J, Mathur EJ, Short JM, Keller M (2002) Cultivating the uncultured. Proceed Nat Acad of Sci USA 99:15681–15686CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • V. Kumar
    • 1
    Email author
  • D. Rao
    • 1
  • T. Thomas
    • 2
  • S. Kjelleberg
    • 2
  • S. Egan
    • 2
  1. 1.Division of Biology, School of Biological and Chemical Sciences, Faculty of Science, Technology and EnvironmentUniversity of the South PacificSuvaFiji
  2. 2.School of Biotechnology and Biomolecular Sciences and the Centre for Marine Bio-InnovationUniversity of New South WalesSydneyAustralia

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