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Effects of 2E,4E-Decadienal on Motility and Aggregation of Diatoms and on Biofilm Formation

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Abstract

Phototrophic biofilm formation and dynamics result from the interaction between several parameters, including chemical interactions. Some of the secondary metabolites released by microalgae can influence the composition of benthic communities. We determined the effects of decadienal (DD), a polyunsaturated aldehyde produced by diatoms, on a benthic diatom, Fistulifera saprophila. At 5 μg ml−1, DD reduced cell motility by 88% and cell adhesion to the substrate by 91%. The effects occurred in less than 30 min. Using a fluorescent probe, we showed that DD could induce nitric oxide (NO) accumulation in F. saprophila cells. Cells exposed to a NO donor presented reduced adhesion and motility, which suggests the involvement of this cellular messenger in the mode of action of DD. Short-term experiments in microcosms showed that the presence of DD on a substrate strongly inhibited biofilm formation. Moreover, when the biofilm was bispecific, DD modified the proportion of the two species present. This indicates that the presence of DD-producing diatoms in a biofilm may favor the presence of certain microalgae at the expense of others. In addition to the effects on adhesion and motility, DD induced the formation of aggregates of F. saprophila cells. Aggregation was independent of NO production. Complementary experiments were performed with two other benthic diatoms, Nitzschia palea and Mayamea atomus. They showed that the effects of DD on adhesion and aggregation were species-dependent.

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References

  1. Adolph S, Bach S, Blondel M, Cueff A, Moreau M, Pohnert G, Poulet SA, Wichard T, Zuccaro A (2004) Cytotoxicity of diatom-derived oxylipins in organisms belonging to different phyla. J Exp Biol 207:2935–2946

    Article  CAS  PubMed  Google Scholar 

  2. Bates SS, Bird CJ, de Freitas ASW, Foxall R, Gilgan M, Hanic LA, Johnson GR, McCulloch AW, Odense P, Pocklington R, Quilliam MA, Sim PG, Smith JC, Rao DVS, Todd ECD, Walter JA, Wright JLC (1989) Pennate diatom Nitzschia pungens as the primary source of domoic acid, a toxin in shellfish from eastern Prince Edward Island, Canada. Can J Fish Aquat Sci 46:1203–1215

    Article  CAS  Google Scholar 

  3. Caldwell GS, Olive PJW, Bentley MG (2002) Inhibition of embryonic development and fertilization in broadcast spawning marine invertebrates by water soluble diatom extracts and the diatom toxin 2-trans, 4-trans decadienal. Aquat Toxicol 60:123–137

    Article  CAS  PubMed  Google Scholar 

  4. Casotti R, Mazza S, Brunet C, Vantrepotte V, Ianora A, Miralto A (2005) Growth inhibition and toxicity of the diatom aldehyde 2-trans, 4-trans-decadienal on Thalassiosira weissflogii (Bacillariophyceae). J Phycol 41:7–20

    Article  CAS  Google Scholar 

  5. Chiovitti A, Dugdale TM, Wetherbee R (2006) Diatom adhesives: molecular and mechanical properties. In: Smith AM, Callow JA (eds) Biological adhesives. Springer, Heidelberg, pp 79–103

    Chapter  Google Scholar 

  6. Cooksey KE, Wigglesworth-Cooksey B (1995) Adhesion of bacteria and diatoms to surfaces in the sea: a review. Aquat Microb Ecol 9:87–96

    Article  Google Scholar 

  7. Cutignano A, d’Ippolito G, Romano G, Lamari N, Cimino G, Febbraio F, Fontana A (2006) Chloroplastic glycolipids fuel aldehyde biosynthesis in the marine diatom Thalassiosira rotula. Chembiochem 7:450–456

    Article  CAS  PubMed  Google Scholar 

  8. Desbois AP, Mearns-Spragg A, Smith VJ (2009) A fatty acid from the diatom Phaeodactylum tricornutum is antibacterial against diverse bacteria including multi-resistant Staphylococcus aureus (MRSA). Mar Biotechnol 11:45–52

    Article  CAS  PubMed  Google Scholar 

  9. Eulin A, Le Cohu R (1998) Epilithic diatom communities during the colonization of artificial substrates in the river Garonne (France). Comparison with the natural communities. Arch Hydrobiol 143:79–106

    Google Scholar 

  10. Feminella JW, Resh VH (1991) Herbivorous caddisflies, macroalgae, and epilithic microalgae: dynamic interactions in a stream grazing system. Oecologia 87:247–256

    Article  Google Scholar 

  11. Feminella JW, Hawkins CP (1995) Interactions between stream herbivores and periphyton: a quantitative analysis of past experiments. J North Am Benthol Soc 14:465–509

    Article  Google Scholar 

  12. Fontana A, D’Ippolito G, Cutignano A, Miralto A, Ianora A, Romano G, Cimino G (2007) Chemistry of oxylipin pathways in marine diatoms. Pure Appl Chem 79:475–484

    Article  Google Scholar 

  13. Hart DD (1985) Grazing insects mediate algal interactions in a stream benthic community. Oikos 44:40–46

    Article  Google Scholar 

  14. Jüttner F, Dürst U (1997) High lipoxygenase activities in epilithic biofilms of diatoms. Arch Hydrobiol 138:451–463

    Google Scholar 

  15. Jüttner F (1999) Allelochemical control of natural photoautotrophic biofilms. In: Keevil CW, Godfree A, Holt D, Dow C (eds) Biofilms in aquatic environment. Royal Society of Chemistry, Cambridge, pp 43–50

    Google Scholar 

  16. Jüttner F (2001) Liberation of 5, 8, 11, 14, 17-eicosapentaenoic acid and other polyunsaturated fatty acid from lipids as a grazer defence reaction in epilithic diatom biofilm. J Phycol 37:744–755

    Article  Google Scholar 

  17. Jüttner F (2005) Evidence that polyunsaturated aldehydes of diatom are repellents for pelagic crustacean grazers. Aquat Ecol 39:271–282

    Article  Google Scholar 

  18. Kilham SS, Kreeger DA, Lynn SG, Goulden CE, Herrera L (1998) COMBO: a defined freshwater culture medium for algae and zooplankton. Hydrobiologia 377:147–159

    Article  CAS  Google Scholar 

  19. Larned ST (2010) A prospectus for periphyton: recent and future ecological research. J North Am Benthol Soc 29:182–206

    Google Scholar 

  20. Leflaive J, Boulêtreau S, Buffan-Dubau E, Ten-Hage L (2008) Temporal patterns in epilithic biofilms—relation with a putative allelopathic activity. Fundam Appl Limnol 173:121–134

    Article  CAS  Google Scholar 

  21. Leflaive J, Buffan-Dubau E, Ten-Hage L (2008) Algal bioactive compounds reduce net oxygen fluxes of artificial diatom biofilms. Aquat Microb Ecol 51:276–284

    Article  Google Scholar 

  22. Leflaive J, Ten-Hage L (2009) Allelopathic interactions in benthic biofilms: effects of abiotic conditions on production of and sensitivity to allelochemicals. J North Am Benthol Soc 28:271–280

    Article  Google Scholar 

  23. Lock MA (1993) Attached microbial communities in rivers. In: Ford TE (ed) Aquatic microbiology—an ecological approach. Blackwell Scientific Publications, Oxford, pp 113–138

    Google Scholar 

  24. Lürling M, Van Donk E (1996) Zooplancton-induced unicell-colony transformation in Scenedesmus acutus and its effect on growth of herbivore Daphnia. Oecologia 108:432–437

    Article  Google Scholar 

  25. Mc Cormick PV, Stevenson R (1991) Mechanisms of benthic algal succession in lotic environments. Ecology 72:1835–1848

    Article  Google Scholar 

  26. McLachlan JL, Brownlee C, Taylor AR, Geider RJ, Underwood GJC (2009) Light-induced motile reponses of the estuarine benthic diatoms Navicula perminuta and Cylindrotheca closterium (Bacyllariophyceae). J Phycol 45:592–599

    Article  Google Scholar 

  27. Miralto A, Barone G, Romano G, Poulet SA, Ianora A, Russo GL, Buttino I, Mazzarella G, Laabir M, Gabrini M, Giacobbe MG (1999) The insidious effect of diatoms on copepod reproduction. Nature 402:173–176

    Article  CAS  Google Scholar 

  28. Molino PJ, Wetherbee R (2008) The biology of biofouling diatoms and their role in the development of microbial slimes. Biofouling 24:365–379

    Article  CAS  PubMed  Google Scholar 

  29. Pohnert G (2000) Wound-activated chemical defense in unicellular planktonic algae. Angew Chem-Int Edit 39:4352–4354

    CAS  Google Scholar 

  30. Pohnert G (2002) Phospholipase A2 activity triggers the wound-activated chemical defense in the diatom Thalassiosira rotula. Plant Physiol 129:103–111

    Article  CAS  PubMed  Google Scholar 

  31. Pohnert G, Steinke M, Tollrian R (2007) Chemical cues, defence metabolites and the shaping of pelagic interspecific interactions. Trends Ecol Evol 22:198–204

    Article  PubMed  Google Scholar 

  32. Poulsen NC, Spector I, Spurck TP, Schultz TF, Wetherbee R (1999) Diatom gliding is the result of an actin-myosin motility system. Cell Motil Cytoskel 44:23–33

    Article  CAS  Google Scholar 

  33. Ribalet F, Berges JA, Ianora A, Casotti R (2007) Growth inhibition of cultured marine phytoplankton by toxic algal-derived polyunsaturated aldehydes. Aquat Toxicol 85:219–227

    Article  CAS  PubMed  Google Scholar 

  34. Ribalet F, Intertaglia L, Lebaron P, Casotti R (2008) Differential effect of three polyunsaturated aldehydes on marine bacterial isolates. Aquat Toxicol 86:249–255

    Article  CAS  PubMed  Google Scholar 

  35. Stevenson R, Bothwell M, Lowe R (1996) Algal ecology: freshwater benthic ecosystems. Academic, San Diego

    Google Scholar 

  36. Thompson SEM, Taylor AR, Brownlee C, Callow ME, Callow GA (2008) The role of nitric oxide in diatom adhesion in relation to substratum properties. J Phycol 44:967–976

    Article  CAS  Google Scholar 

  37. Underwood GJC, Paterson DM (2003) The importance of extracellular carbohydrate production by marine epipelic diatoms. Adv Bot Res 40:183–240

    Article  CAS  Google Scholar 

  38. Vardi A, Formiggini F, Casotti R, De Martino A, Ribalet F, Miralto A, Bowler C (2006) A stress surveillance system based on calcium and nitric oxide in marine diatoms. PLoS Biol 4:411–419

    Article  CAS  Google Scholar 

  39. Vardi A, Bidle KD, Kwityn C, Hirsh DJ, Thompson SM, Callow JA, Falkowski PG, Bowler C (2008) A diatom gene regulating nitric-oxide signaling and susceptibility to diatom-derived aldehydes. Curr Biol 18:895–899

    Article  CAS  PubMed  Google Scholar 

  40. Vreeland V, Waite JH, Epstein L (1998) Polyphenols and oxidases in susbtratum adhesion by marine algae and mussels. J Phycol 34:1–8

    Article  CAS  Google Scholar 

  41. Wang R, Shimizu Y (1990) Bacillariodes I and II, a new type of cyclopentane eicosanoids from the diatom Nitzschia pungens. J Chem Soc-Chem Com 5:413–414

    Google Scholar 

  42. Watson SB, Satchwill T, Dixon E, McCauley E (2001) Under-ice blooms and source-water odour in a nutrient-poor resevoir: biological, ecological and applied perspectives. Freshwat Biol 46:1553–1567

    Article  CAS  Google Scholar 

  43. Wetherbee R, Lind JL, Burke J, Quatrano RS (1998) The first kiss: establishment and control of initial adhesion by raphid diatoms. J Phycol 34:9–15

    Article  Google Scholar 

  44. Wichard T, Poulet SA, Halsband-Lenk C, Albaina A, Harris R, Liu D, Pohnert G (2005) Survey of the chemical defence potential in diatoms: screening of fifty one species for α, β, γ, δ-unsaturated aldehydes. J Chem Ecol 31:949–958

    Article  CAS  PubMed  Google Scholar 

  45. Wiltshire K, Boersma M, Meyer B (2003) Grazer-induced changes in the desmid Staurastrum. Hydrobiologia 491:255–260

    Article  Google Scholar 

Download references

Acknowledgments

This work was funded by the French National Program EC2CO (Environmental Microbiology, 2008, 2009). We are grateful to Jessica Ferriol and Solveig Carpentier for their assistance.

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Correspondence to Joséphine Leflaive.

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Leflaive, J., Ten-Hage, L. Effects of 2E,4E-Decadienal on Motility and Aggregation of Diatoms and on Biofilm Formation. Microb Ecol 61, 363–373 (2011). https://doi.org/10.1007/s00248-010-9755-x

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  • DOI: https://doi.org/10.1007/s00248-010-9755-x

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