Chemical interactions in diatoms: Role of polyunsaturated aldehydes and precursors

New Phytologist

Volumn 184, Issue 4, 2009, Pages 794-805

  Leflaive, Joséphine ^a   Ten Hage, Loïc ^a  

^a UNIVERSITÉ DE TOULOUSE   (France)

Author keywords

Allelopathy; Chemical interactions; Diatoms; Infochemical; Polyunsaturated aldehydes (PUAs); Polyunsaturated fatty acids (PUFAs); Predator defence

Indexed keywords

ALDEHYDE;

ALDEHYDE; ALGA; ALLELOPATHY; ANTIPREDATOR DEFENSE; BIOACTIVITY; BIOCHEMISTRY; CHEMICAL CUE; CHEMICAL DEFENSE; COMMUNITY STRUCTURE; CRUSTACEAN; DIATOM; INTERSPECIFIC INTERACTION; METABOLITE; REPRODUCTIVE SUCCESS;

CHEMICAL STRUCTURE; CHEMISTRY; DIATOM; ECOSYSTEM; METABOLISM; REVIEW;

ALDEHYDES; DIATOMS; ECOSYSTEM; MOLECULAR STRUCTURE;

ALGAE; BACILLARIOPHYTA; COPEPODA;

EID: 70449361906     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2009.03033.x     Document Type: Review

References (103)

1. Adolph S, Poulet SA, Pohnert G. 2003. Synthesis and biological activity of α,β,γ,δ-unsaturated aldehydes from diatoms. Tetrahedron 59 : 3003 3008.
2. 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. Journal of Experimental Biology 207 : 2935 2946.
3. Akakabe Y, Matsui K, Kajiwara T. 2003. 2,4-Decadienals are produced via (R)-11-HPITE from arachidonic acid in marine green alga Ulva conglobata. Bioorganic & Medicinal Chemistry 11 : 3607 3609.
4. Armbrust V, Berges JA, Bowler C, Green BR, Martinez D, Putnam NH, Zhou SG, Allen AE, Apt KE, Bechner M et al. 2004. The genome of the diatom Thalassiosira pseudonana: ecology, evolution and metabolism. Science 306 : 79 86.
5. Ban S, Burns C, Castel J, Chaudron Y, Christou E, Escribano R, Fonda Umani S, Gasparini S, Guerrero Ruiz F, Hoffmeyer M et al. 1997. The paradox of diatom-copepod interactions. Marine Ecology Progress Series 157 : 287 293.
6. Benkendorff K, Davis AR, Rogers CN, Bremner JB. 2005. Free fatty acids and sterols in the benthic spawn of aquatic molluscs, and their associated antimicrobial properties. Journal of Experimental Marine Biology and Ecology 316 : 29 44.
7. Berges JA, Falkowski PG. 1998. Physiological stress and cell death in marine phytoplankton: induction of protease in response to nitrogen or light limitation. Limnology and Oceanography 43 : 129 135.
8. Bidle KD, Bender S. 2008. Activation of metacaspase and programmed cell death in the marine diatom, Thalassiosira pseudonana. Eukaryotic Cell 7 : 223 236.
9. Bidle KD, Falkowski PG. 2004. Cell death in planktonic, photosynthetic microorganisms. Nature Reviews Microbiology 2 : 643 655.
10. Bisignano G, Lagana MG, Trombetta D, Arena A, Nostro A, Uccella N, Mazzanti G, Saija A. 2001. In vitro antibacterial activity of some aliphatic aldehydes from Olea europaea L. FEMS Microbiology Letters 198 : 9 13.
11. Bowler C, Allen AE, Badger HJ, Grimwood J, Jabbari K, Kuo A, Maheswari U, Martens C, Maumus F, Otillar RP et al. 2008. The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature 456 : 239 244.
12. Buttino I, de Rosa G, Carotenuto Y, Mazzela M, Ianora A, Esposito F, Vitiello V, Quaglia F, La Rotonda MI, Miralto A. 2008. Aldehyde-encapsulating liposomes impair marine grazer survivorship. Journal of Experimental Biology 211 : 1426 1433.
13. 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. Aquatic Toxicology 60 : 123 137.
14. Caldwell GS, Bentley MG, Olive PJW. 2003. The use of a brine shrimp (Artemia salina) bioassay to assess the toxicity of diatom extracts and short chain aldehydes. Toxicon 42 : 301 306.
15. Caldwell GS, Bentley MG, Olive PJW. 2004. First evidence of sperm motility inhibition by the diatom aldehyde 2,E-4,E-decadienal. Marine Ecology Progress Series 273 : 97 108.
16. Carotenuto Y, Lampert W. 2004. Ingestion and incorporation of freshwater diatoms by Daphnia pulicaria: do morphology and oxylipin production matter? Journal of Plankton Research 26 : 563 569.
17. Carotenuto Y, Wichard T, Pohnert G, Lampert W. 2005. Life-history responses of Daphnia pulicaria to diets containing freshwater diatoms: effects of nutritional quality versus polyunsaturated aldehydes. Limnology and Oceanography 50 : 449 454.
18. 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). Journal of Phycology 41 : 7 20.
19. Ceballos S, Ianora A. 2003. Different diatoms induce contrasting effects on the reproductive success of the copepod Temora stylifera. Journal of Experimental Marine Biology and Ecology 294 : 189 202.
20. 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.
21. D'Ippolito G, Iadicicco I, Romano G, Fontana A. 2002. Detection of short-chain aldehydes in marine organism: the diatom Thalassiosira rotula. Tetrahedron Letters 43 : 6137 6140.
22. D'Ippolito G, Romano G, Caruso T, Spinella A, Cimino G, Fontana A. 2003. Production of octadienal in the marine diatom Skeletonema costatum. Organic Letters 5 : 885 887.
23. Delledonne M, Xia Y, Dixon RA, Lamb C. 1998. Nitric oxide functions as a signal in plant disease. Nature 394 : 585 588.
24. Desbois AP, Lebl T, Yan LM, Smith VJ. 2008. Isolation and structural characterisation of two antibacterial free fatty acids from the marine diatom Phaeodactylum tricornutum. Applied Microbiology and Biotechnology 81 : 755 764.
25. 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). Marine Biotechnology 11 : 45 52.
26. Dicke M, Sabelis MW. 1988. Infochemicals terminology: based on cost-benefit analysis rather than origin of compounds? Functional Ecology 2 : 131 139.
27. Dutz J, Koski M, Jonasdottir S. 2008. Copepod reproduction is unaffected by diatom aldehyde or lipid composition. Limnology and Oceanography 53 : 225 235.
28. Feminella JW, Hawkins CP. 1995. Interactions between stream herbivores and periphyton: a quantitative analysis of past experiments. Journal of the North American Benthological Society 14 : 465 509.
29. Flynn KJ, Irigoien X. 2009. Aldehyde-induced insidious effects cannot be considered as a diatom defence mechanism against copepods. Marine Ecology - Progress Series 377 : 79 89.
30. Fontana A, d'Ippolito G, Cutignano A, Romano G, Lamari N, Gallucci AM, Miralto A, Ianora A. 2007. LOX-induced lipid peroxidation mechanism responsible for the detrimental effect of marine diatoms on zooplankton grazers. ChemBioChem 8 : 1810 1818.
31. Franklin DJ, Brussaard CPD, Berges JA. 2006. What is the role and nature of programmed cell death in phytoplankton ecology? European Journal of Phycology 41 : 1 14.
32. Fu M, Koulman A, van Rijssel M, Lutzen A, de Boer MK, Liebezeit G. 2004. Chemical characterisation of three haemolytic compounds from the microalgal species Fibrocapsa japonica (Raphidophyceae). Toxicon 43 : 355 363.
33. Guo FQ, Okamoto M, Crawford NM. 2003. Identification of a plant nitric oxide synthase gene involved in hormonal signaling. Science 302 : 100 103.
34. Halsband-Lenk C, Pierson JJ, Leising AW. 2005. Reproduction of Pseudocalanus newmani (Copepoda: Calanoida) is deleteriously affected by diatom blooms - a field study. Progress in Oceanography 67 : 332 348.
35. Hansen E, Eilersten HC. 2007. Do the polyunsaturated aldehydes produced by Phaeocystis pouchetii (Hariot) Lagerheim influence diatom growth during the spring bloom in northern Norway? Journal of Plankton Research 29 : 87 96.
36. Hansen E, Ernstsen A, Eilersten HC. 2004. Isolation and characterisation of a cytotoxic polyunsaturated aldehyde from the marine phytoplankton Phaeocystis pouchetii (Hariot) Lagerheim. Toxicology 199 : 207 217.
37. Hay ME. 2002. The next wave in aquatic chemical ecology. Journal of Chemical Ecology 28 : 1897 1899.
38. Hay ME, Kubanek J. 2002. Community and ecosystem level consequences of chemical cues in the plankton. Journal of Chemical Ecology 28 : 2001 2016.
39. Horner RA, Postel JR, Halsband-Lenk C, Pierson JJ, Pohnert G, Wichard T. 2005. Winter-spring phytoplankton blooms in Dabob Bay, Washington. Progress in Oceanography 67 : 286 313.
40. Ianora A, Poulet SA. 1993. Egg viability of the copepod Temora stylifera. Limnology and Oceanography 38 : 1615 1626.
41. Ianora A, Poulet SA, Miralto A. 2003. The effects of diatoms on copepod reproduction: a review. Phycologia 42 : 351 363.
42. Ianora A, Miralto A, Poulet SA, Carutenuto Y, Buttino I, Romano G, Casotti R, Pohnert G, Wichard T, Colucci-D'Amato L et al. 2004. Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom. Nature 429 : 403 407.
43. Ianora A, Casotti R, Bastianini M, Brunet C, D'Ippolito G, Acri F, Fontana A, Cutignano A, Turner JT, Miralto A. 2008. Low reproductive success for copepods during a bloom of the non-aldehyde-producing diatom Cerataulina pelagica in the North Adriatic Sea. Marine Ecology - An Evolutionary Perspective 29 : 399 410.
44. Irigoien X, Harris RP, Head RN, Harbour D. 2000. The influence of diatom abundance on the egg production rate of Calanus helgolandicus in the English Channel. Limnology and Oceanography 45 : 1433 1439.
45. Irigoien X, Harris RP, Verheye HM, Joly P, Runge J, Starr M, Pond D, Campbell R, Shreeve R, Ward P et al. 2002. Copepod hatching success in marine ecosystem with high diatom concentrations. Nature 419 : 387 389.
46. Jones RH, Flynn KJ. 2005. Nutritional status and diet composition affect the value of diatoms as copepod prey. Science 307 : 1457 1459.
47. Jüttner F. 1981. Detection of lipid degradation products in the water of a reservoir during a bloom of Synura uvella. Applied and Environmental Microbiology 41 : 100 106.
48. Jüttner F. 1999. Allelochemical control of natural photoautotrophic biofilms. In : Keevil CW, Godfree A, Holt D, Dow C, eds. Biofilms in aquatic environment. Cambridge, UK : Royal Society of Chemistry, 43 50.
49. Jüttner F. 2001. Liberation of 5,8,11,14,17-eicosapentaenoic acid and other polyunsaturated fatty acids from lipids as a grazer defence reaction in epilithic diatom biofilm. Journal of Phycology 37 : 744 755.
50. Jüttner F. 2005. Evidence that polyunsaturated aldehydes of diatom are repellents for pelagic crustacean grazers. Aquatic Ecology 39 : 271 282.
51. Jüttner F, Dürst U. 1997. High lipoxygenase activities in epilithic biofilms of diatoms. Archiv für Hydrobiologie 138 : 451 463.
52. Keating KI. 1977. Allelopathic influence on blue-green bloom sequence in a eutrophic lake. Science 196 : 885 887.
53. Laabir M, Poulet SA, Ianora A, Miralto A, Cueff A. 1995. Reproductive response of Calanus helgolandicus. 2. In situ inhibition of embryonic development. Marine Ecology - Progress Series 129 : 97 105. (Pubitemid 26454183)
54. Lane N. 2008. Origins of death. Nature 453 : 583 585.
55. Leflaive J, Ten-Hage L. 2007. Algal and cyanobacterial secondary metabolites in freshwaters: a comparison of allelopathic compounds and toxins. Freshwater Biology 52 : 199 214.
56. Leflaive J, Buffan-Dubau E, Ten-Hage L. 2008. Algal bioactive compounds reduce net oxygen fluxes of artificial diatom biofilms. Aquatic Microbial Ecology 51 : 276 284.
57. Legrand C, Rengefors K, Fistarol GO, Granéli E. 2003. Allelopathy in phytoplankton - biochemical, ecological and evolutionary aspects. Phycologia 42 : 406 419.
58. McClintock JB, Baker BJ. 2001. Marine chemical ecology. London, UK : CRC Press.
59. Miralto A, Barone G, Romano G, Poulet SA, Ianora A, Russo GL, Buttino I, Mazzarella G, Laabir M, Gabrini M et al. 1999. The insidious effect of diatoms on copepod reproduction. Nature 402 : 173 176.
60. Paffenhöfer GA. 2002. An assessment of the effects of diatoms on planktonic copepods. Marine Ecology - Progress Series 227 : 305 310.
61. Paffenhöfer GA, Ianora A, Miralto A, Turner JT, Kleppel GS, d'Alcala MR, Casotti R, Caldwell GS, Pohnert G, Fontana A et al. 2005. Colloquium on diatom-copepod interactions. Marine Ecology - Progress Series 286 : 293 305.
62. Paul VJ, Arthur KE, Ritson-Williams R., Ross C, Sharp K. 2007. Chemical defenses: from compounds to communities. Biological Bulletin 213 : 226 251.
63. Pierson JJ, Halsband-Lenk C, Leising AW. 2005. Reproductive success of Calanus pacificus during diatom blooms in Dabob Bay, Washington. Progress in Oceanography 67 : 314 331.
64. Pohnert G. 2000. Wound-activated chemical defense in unicellular planktonic algae. Angewandte Chemie-International Edition 39 : 4352 4354.
65. Pohnert G. 2002. Phospholipase A2 activity triggers the wound-activated chemical defense in the diatom Thalassiosira rotula. Plant Physiology 129 : 103 111.
66. Pohnert G. 2005. Diatom\copepod interactions in plankton: the indirect chemical defense of unicellular algae. ChemBioChem 6 : 946 959.
67. Pohnert G, Lumineau O, Cueff A, Adolph S, Cordevant C, Lange M, Poulet S. 2002. Are volatile unsaturated aldehydes from diatoms the main line of chemical defense against copepods? Marine Ecology Progress Series 245 : 33 45.
68. Pohnert G, Steinke M, Tollrian R. 2007. Chemical cues, defence metabolites and the shaping of pelagic interspecific interactions. Trends in Ecology and Evolution 22 : 198 204.
69. Poulet SA, Ianora A, Miralto A, Meijer L. 1994. Do diatoms arrest embryonic-development in copepods. Marine Ecology Progress Series 111 : 79 86.
70. Poulet SA, Laabir M, Ianora A, Miralto A. 1995. Reproductive response of Calanus helgolandicus. 1. Abnormal embryonic and naupliar development. Marine Ecology - Progress Series 129 : 85 95. (Pubitemid 26454182)
71. Poulet SA, Wichard T, Ledoux JB, Lebreton B, Marchetti J, Dancie C, Bonnet D, Cueff A, Morin P, Pohnert G. 2006. Influence of diatoms on copepod reproduction. I. Field and laboratory observations related to Calanus helgolandicus egg production. Marine Ecology - Progress Series 308 : 129 142.
72. Poulet SA, Cueff A, Wichard T, Marchetti J, Dancie C, Pohnert G. 2007a. Influence of diatoms on copepod reproduction. III. Consequences of abnormal oocyte maturation on reproductive factors in Calanus helgolandicus. Marine Biology 152 : 415 428.
73. Poulet SA, Escribano R, Hidalgo P, Cueff A, Wichard T, Aguilera V, Vargas CA, Pohnert G. 2007b. Collapse of Callanus chilensis reproduction in marine environment with high diatom concentration. Journal of Experimental Marine Biology and Ecology 352 : 187 199.
74. Poulson KL, Sieg RD, Kubanek J. 2009. Chemical ecology in the marine plankton. Natural Product Report 26 : 729 745.
75. Refsgaard HHF, Tasai L, Stadtman ER. 2000. Modifications of proteins by polyunsaturated fatty acid peroxidation products. Proceedings of the National Academy of Sciences, USA 97 : 611 616.
76. Ribalet F, Berges JA, Ianora A, Casotti R. 2007a. Growth inhibition of cultured marine phytoplankton by toxic algal-derived polyunsaturated aldehydes. Aquatic Toxicology 85 : 219 227.
77. Ribalet F, Wichard T, Pohnert G, Ianora A, Miralto A, Casotti R. 2007b. Age and nutrient limitation enhance polyunsaturated aldehyde production in marine diatoms. Phytochemistry 68 : 2059 2067.
78. Ribalet F, Intertaglia L, Lebaron P, Casotti R. 2008. Differential effect of three polyunsaturated aldehydes on marine bacterial isolates. Aquatic Toxicology 86 : 249 255.
79. Rice EL. 1984. Allelopathy. New York, NY, USA : Academic Press.
80. Riley GA. 1947. A theoretical analysis of the zooplankton population on Georges Bank. Journal of Marine Research 6 : 104 113.
81. Rittschof D, Cohen JH. 2004. Crustacean peptide and peptide like pheromones and kairomones. Peptides 25 : 1503 1516.
82. Romano G, Russo GL, Buttino I, Ianora A, Miralto A. 2003. A marine diatom-derived aldehyde induces apoptosis in copepod and sea urchin embryos. Journal of Experimental Biology 206 : 3487 3494.
83. Sommer U. 2009. Copepod growth and diatoms: insensitivity of Acartia tonsa to the composition of semi-natural plankton mixtures manipulated by silicon : nitrogen ratios in mesocosms. Oecologia 159 : 207 215.
84. Takamo K, Igarashi S, Mikami H, Hino S. 2003. Causation of reversal simultaneity for diatom biomass and density of Phormidium tenue during the warm season in eutrophic Lake Barato, Japan. Limnology 4 : 73 78.
85. Taylor RL, Caldwell DE, Dunstan HJ, Bentley MG. 2007. Short-term impact of polyunsaturated aldehyde producing diatoms on the harpacticoid copepod, Tisbe holothuriae. Journal of Experimental Marine Biology and Ecology 341 : 60 69.
86. Thompson SEM, Taylor AR, Brownlee C, Callow ME, Callow GA. 2008. The role of nitric oxide in diatom adhesion in relation to substratum properties. Journal of Phycology 44 : 967 976.
87. Tosti E, Romano G, Buttino I, Cuomo A, Ianora A, Miralto A. 2003. Bioactive aldehydes from diatoms block the fertilization current in ascidian oocytes. Molecular Reproduction and Development 66 : 72 80.
88. Turner JT, Ianora A, Miralto A, Laabir M, Esposito F. 2001. Decoupling of copepod grazing rates, fecundity and egg-hatching success on mixed and alternating diatom and dinoflagellate diets. Marine Ecology Progress Series 220 : 187 199.
89. 2 limitation and oxidative stress. Current Biology 9 : 1061 1064.
90. 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 Biology 4 : 411 419.
91. 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. Current Biology 18 : 895 899.
92. Vargas CA, Escribano R, Poulet SA. 2006. Phytoplankton food quality determines time windows for successful zooplankton reproductive pulses. Ecology 87 : 2992 2999.
93. Vidoudez C, Pohnert G. 2008. Growth phase-specific release of polyunsaturated aldehydes by the diatom Skeletonema marinoi. Journal of Plankton Research 30 : 1305 1313.
94. Vollenweider S, Weber H, Stolz S, Chetelat A, Farmer EE. 2000. Fatty acids ketodienes and fatty acids ketotrienes: Michael addition acceptors that accumulate in wounded and diseased Arabidopsis leaves. Plant Journal 24 : 467 476.
95. Wang L-L, Johnson EA. 1992. Inhibition of Listeria monocytogenes by fatty acids and monoglycerides. Applied and Environmental Microbiology 58 : 624 629.
96. Watson SB. 2003. Cyanobacterial and eukaryotic algal odour compounds: signal or by-products? A review of their biological activity. Phycologia 42 : 332 350.
97. Watson SB, Jüttner F, Koster O. 2007. Daphnia behavioral response to taste and odour compounds: ecological significance and application as an inline treatment plant monitoring tool. Water Science and Technology 55 : 23 31.
98. Wendel T, Jüttner F. 1996. Lipoxygenase-mediated formation of hydrocarbons and unsaturated aldehydes in freshwater diatoms. Phytochemistry 41 : 1445 1449.
99. Wichard T, Poulet SA, Halsband-Lenk C, Albaina A, Harris RP, 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. Journal of Chemical Ecology 31 : 949 958.
100. Wichard T, Gerecht A, Boersma M, Poulet SA, Wiltshire K, Pohnert G. 2007. Lipid and fatty acid composition of diatoms revisited: rapid wound-activated change of food quality parameters influences herbivorous copepod reproductive success. ChemBioChem 8 : 1146 1153.
101. Wichard T, Poulet SA, Boulesteix AL, Ledoux JB, Lebreton B, Marchetti J, Pohnert G. 2008. Influence of diatoms on copepod reproduction. II. Uncorrelated effect of diatom-derived alpha,beta,gamma,delta-unsaturated aldehydes and polyunsaturated fatty acids on Calanus helgolandicus in the field. Progress in Oceanography 77 : 30 44.
102. Wolfe-Simon F, Starovoytov V, Reinfelder JR, Schofield O, Falkowski PG. 2006. Localisation and role of manganese superoxide dismutase in a marine diatom. Plant Physiology 142 : 1701 1709.
103. Yamasaki Y, Nagasoe S, Matsubara T, Shikata T, Shimasaki Y, Oshima Y, Honjo T. 2007. Allelopathic interactions between the bacillariophyte Skeletonema costatum and the raphidophyte Heterosigma akashiwo. Marine Ecology Progress Series 339 : 83 92.