Biochemical trade-offs: Evidence for ecologically linked secondary metabolism of the sponge oscarella balibaloi

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Ivanisevic, Julijana ^a,b   Thomas, Olivier P ^b   Pedel, Laura ^a   Pénez, Nicolas ^c   Ereskovsky, Alexander V ^a   Culioli, Gérald ^c   Pérez, Thierry ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

^c UNIVERSITÉ DE TOULON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

SEA WATER;

ARTICLE; AUTUMN; BIOCHEMISTRY; CONTROLLED STUDY; EMBRYO DEVELOPMENT; ENVIRONMENTAL FACTOR; LARVAL DEVELOPMENT; METABOLISM; NONHUMAN; ORGANISMAL INTERACTION; PHENOTYPE; REPRODUCTIVE EFFORT; SEASONAL VARIATION; SPONGE (PORIFERA); SPRING; SUMMER; WATER TEMPERATURE; ANIMAL; ECOSYSTEM; METABOLOME; REPRODUCTION; TEMPERATURE; TIME;

HOMOSCLEROMORPHA; INVERTEBRATA; OSCARELLA;

ANIMALS; ECOSYSTEM; METABOLOME; PHENOTYPE; PORIFERA; REPRODUCTION; SEAWATER; TEMPERATURE; TIME FACTORS;

EID: 81755176117     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028059     Document Type: Article

References (67)

1. Wink M, (2003) Evolution of secondary metabolites from an ecological and molecular phylogenetic perspective. Phytochemistry 64: 3-19.
2. Lopez-Legentil S, Bontemps-Subielos N, Turon X, Banaigs B, (2007) Secondary metabolite and inorganic contents in Cystodytes sp. (Ascidiacea): temporal patterns and association with reproduction and growth. Marine Biology 151: 293-299.
3. Becerro MA, Turon X, Uriz MJ, (1997) Multiple functions for secondary metabolites in encrusting marine invertebrates. Journal of Chemical Ecology 23: 1527-1547.
4. Cronin G, (2001) Resource allocation in seaweeds and marine invertebrates: chemical defense patterns in relation to defence theories. In: McClintock JB, Baker BJ, editors. Marine Chemical Ecology Boca Raton London New York Washington CRC Press pp. 325-353.
5. Dewick PM, eds. (2002) Medicinal natural products: a biosynthetic approach. New York John Wiley & Sons pp. 7-34.
6. Takken W, Dicke M, (2006) Chemical ecology- A multidisciplinary approach. Chemical Ecology: From Gene to Ecosystem 16: 1-8.
7. Coma R, Ribes M, (2003) Seasonal energetic constraints in Mediterranean benthic suspension feeders: effects at different levels of ecological organization. Oikos 101: 205-215.
8. Uriz MJ, Turon X, Becerro MA, Galera J, (1996) Feeding deterrence in sponges. The role of toxicity, physical defenses, energetic contents, and life-history stage. Journal of Experimental Marine Biology and Ecology 205: 187-204.
9. Lopez-Legentil S, Bontemps-Subielos N, Turon X, Banaigs B, (2006) Temporal variation in the production of four secondary metabolites in a colonial ascidian. Journal of Chemical Ecology 32: 2079-2084.
10. Turon X, Tarjuelo I, Uriz MJ, (1998) Growth dynamics and mortality of the encrusting sponge Crambe crambe (Poecilosclerida) in contrasting habitats: correlation with population structure and investment in defence. Functional Ecology 12: 631-639.
11. Uriz MJ, Turon X, Becerro MA, Galera J, Lozano J, (1995) Patterns of resource-allocation to somatic, defensive and reproductive functions in the Mediterranean encrusting sponge Crambe crambe (Demospongiae, Poecilosclerida) Marine Ecology Progress Series 124: 159-170.
12. Becerro MA, Thacker RW, Turon X, Uriz MJ, Paul VJ, (2003) Biogeography of sponge chemical ecology: comparisons of tropical and temperate defenses. Oecologia 135: 91-101.
13. Marti R, Fontana A, Uriz MJ, Cimino G, (2003) Quantitative assessment of natural toxicity in sponges: Toxicity bioassay versus compound quantification. Journal of Chemical Ecology 29: 1307-1318.
14. Turon X, Becerro MA, Uriz MJ, Llopis J, (1996) Small scale association measures in epibenthic communities as a clue for allelochemical interactions. Oecologia 108: 351-360.
15. Page M, West L, Northcote P, Battershill C, Kelly M, (2005) Spatial and temporal variability of cytotoxic metabolites in populations of the New Zealand sponge Mycale hentscheli. Journal of Chemical Ecology 31: 1161-1174.
16. Abdo DA, Motti CA, Battershill CN, Harvey ES, (2007) Temperature and spatiotemporal variability of salicylihalamide A in the sponge Haliclona sp. Journal of Chemical Ecology 33: 1635-1645.
17. Marti R, Uriz MJ, Turon X, (2004) Seasonal and spatial variation of species toxicity in Mediterranean seaweed communities: correlation to biotic and abiotic factors. Marine Ecology Progress Series 282: 73-85.
18. Ferretti C, Vacca S, De Ciucis C, Marengo B, Duckworth AR, et al. (2009) Growth dynamics and bioactivity variation of the Mediterranean demosponges Agelas oroides (Agelasida, Agelasidae) and Petrosia ficiformis (Haplosclerida, Petrosiidae). Marine Ecology-an Evolutionary Perspective 30: 327-336.
19. Turon X, Becerro MA, Uriz MJ, (1996) Seasonal patterns of toxicity in benthic invertebrates: The encrusting sponge Crambe crambe (Poecilosclerida). Oikos 75: 33-40.
20. Becerro MA, Turon X, Uriz MJ, (1995) Natural variation of toxicity in encrusting sponge Crambe crambe (Schmidt) in relation to size and environment. Journal of Chemical Ecology 21: 1931-1946.
21. Becerro MA, Uriz MJ, Turon X, (1997) Chemically-mediated interactions in benthic organisms: the chemical ecology of Crambe crambe (Porifera, Poecilosclerida). Hydrobiologia 355: 77-89.
22. Luter HM, Duckworth AR, (2010) Influence of size and spatial competition on the bioactivity of coral reef sponges. Biochemical Systematics and Ecology 38: 146-153.
23. Luter HM, Duckworth AR, Syms C, (2007) Cytotoxic and anti-microbial activity of the sponge Iotrochota sp. as a function of size and spatial competitors. Marine Biology Research 3: 312-318.
24. Maida M, Carroll AR, Coll JC, (1993) Variability of terpene content in the soft coral Sinularia flexibilis (Coelenterata, Octocoralia) and its ecological implicationsJournal of Chemical Ecology 19: 2285-2296.
25. Harvell CD, Fenical W, Roussis V, Ruesink JL, Griggs CC, et al. (1993) Local and geographic variation in the defensive chemistry of a West Indian gorgonian coral (Briareum asbestinum). Marine Ecology Progress Series 93: 165-173.
26. Turon X, Marti R, Uriz MJ, (2009) Chemical bioactivity of sponges along an environmental gradient in a Mediterranean cave. Scientia Marina 73: 387-397.
27. Leong W, Pawlik JR, (2010) Evidence of a resource trade-off between growth and chemical defenses among Caribbean coral reef sponges. Marine Ecology Progress Series 406: 71-78.
28. Pawlik JR, Henkel TP, McMurray SE, Lopez-Legentil S, Loh TL, et al. (2008) Patterns of sponge recruitment and growth on a shipwreck corroborate chemical defense resource trade-off. Marine Ecology-Progress Series 368: 137-143.
29. Viant MR, (2009) Applications of metabolomics to the environmental sciences. Metabolomics 5: 1-2.
30. Bundy JG, Davey MP, Viant MR, (2009) Environmental metabolomics: a critical review and future perspectives. Metabolomics 5: 3-21.
31. Prince EK, Pohnert G, (2010) Searching for signals in the noise: metabolomics in chemical ecology. Analytical and Bioanalytical Chemistry 396: 193-197.
32. Sipkema D, Franssen MCR, Osinga R, Tramper J, Wijffels RH, (2005) Marine sponges as pharmacy. Marine Biotechnology 7: 142-162.
33. Sara M, Vacelet J, (1973) Écologie des Demosponges. In: Grassé PP, editors. Traité de Zoologie, Anatomie, Systématique, Biologie: Spongiaires Paris Masson pp. 462-576.
34. Laborel J, Vacelet J, (1959) Les grottes sous-marines obscures en Méditerranée. Comptes Rendus de l'Académie des Sciences Paris 248: 2619-2621.
35. Laubier L, (1966) Le Coralligène des Albères. Monographie biocénotique. [Thèse Sci. Nat.] Paris Univ. Paris VI.
36. Ballesteros E, (2006) Mediterranean coralligenous assemblages: A synthesis of present knowledge. Oceanography and Marine Biology- an Annual Review 44: 123-130.
37. Pérez T, Ivanisevic J, Dubois M, Pedel L, Thomas OP, et al. (2011) Oscarella balibaloi, a new sponge species (Homoscleromorpha: Plakinidae) from the Western Mediterranean Sea: cytological description, reproductive cycle and ecology. Marine Ecology: An Evolutionary Perspective 32: 174-187.
38. Ivanisevic J, Thomas OP, Lejeusne C, Chevaldonné P, Pérez T, (2011) Metabolic fingerprinting as an indicator of biodiversity: towards understanding inter-specific relationships among Homoscleromorpha sponges. Metabolomics 2: 289-305.
39. Botsford JL, (2002) A comparison of ecotoxicological tests. Atla-Alternatives to Laboratory Animals 30: 539-550.
40. Taylor MW, Schupp PJ, Dahllof I, Kjelleberg S, Steinberg PD, (2004) Host specificity in marine sponge associated bacteria, and potential implications for marine microbial diversity. Environmental Microbiology 6: 121-130.
41. Webster NS, Taylor MW, Behnam F, Lucker S, Rattei T, et al. (2010) Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environmental Microbiology 12: 2070-2082.
42. Webster NS, Cobb RE, Soo R, Anthony SL, Battershill CN, et al. (2011) Bacterial Community Dynamics in the Marine Sponge Rhopaloeides odorabile Under In Situ and Ex Situ Cultivation. Marine Biotechnology 13: 296-304.
43. Webster NS, Taylor MW, (2011) Marine sponges and their microbial symbionts: love and other relationships. Environmental Microbiology (DOI: 10.1111/j.1462-2920.2011.02460.x).
44. Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, et al, Assessing the complex sponge microbiota-core, variable and species-specific bacterial communities in marine sponges. International Society for Microbial Ecology Journal. (in press). (DOI: 10.1038/ismej.2011.116).
45. Vishnyakov AE, Ereskovsky A, (2009) Bacterial symbionts as an additional cytological marker for identification of sponges without a skeleton. Marine Biology 156: 1625-1632.
46. Ivanisevic J, Perez T, Ereskovsky AV, Barnathan G, Thomas OP, (2011) Lysophospholipids in the Mediterranean sponge Oscarella tuberculata: Seasonal variability and putative biological role 37: 537-545.
47. Marti R, Uriz MJ, Turon X, (2005) Spatial and temporal variation of natural toxicity in cnidarians, bryozoans and tunicates in Mediterranean caves. Scientia Marina 69: 485-492.
48. Duckworth AR, Battershill CN, Schiel DR, (2004) Effects of depth and water flow on growth, survival and bioactivity of two temperate sponges cultured in different seasons. Aquaculture 242: 237-250.
49. Dworjanyn SA, Wright JT, Paul NA, de Nys R, Steinberg PD, (2006) Cost of chemical defence in the red alga Delisea pulchra. Oikos 113: 13-22.
50. Baldacconi R, Nonnis-Marzano C, Gaino E, Corriero G, (2007) Sexual reproduction, larval development and release in Spongia officinalis L. (Porifera, Demospongiae) from the Apulian coast. Marine Biology 152: 969-979.
51. Mercurio M, Corriero G, Gaino E, (2007) A 3-year investigation of sexual reproduction in Geodia cydonium (Jameson 1811) (Porifera, Demospongiae) from a semi-enclosed Mediterranean bay. Marine Biology 151: 1491-1500.
52. Engel S, Pawlik JR, (2005) Interactions among Florida sponges. I. Reef habitats. Marine Ecology-Progress Series 303: 133-144.
53. Jackson JBC, Buss L, (1975) Allelopathy and spatial competition among coral-reef invertebrates Proceedings of the National Academy of Sciences of the United States of America 72: 5160-5163.
54. Puyana M, (2002) Chemical ecology of Caribbean sponges of the genus Aplysina. Dissertation Abstracts International Part B: Science and Engineering 62: 5576.
55. Hentschel U, Schmid M, Wagner M, Fieseler L, Gernert C, et al. (2001) Isolation and phylogenetic analysis of bacteria with antimicrobial activities from the Mediterranean sponges Aplysina aerophoba and Aplysina cavernicola. FEMS Microbiology Ecology 35: 305-312.
56. Weiss B, Ebel R, Elbrächter M, Kirchner M, Proksch P, (1996) Defense metabolites from the marine sponge Verongia aerophoba. Biochemical Systematics and Ecology 24: 1-7.
57. Thompson JE, (1985) Exudation of biologically active metabolites in the sponge Aplysina fistularis.1. Biological evidence. Marine Biology 88: 23-26.
58. Thacker RW, Becerro MA, Lumbang WA, Paul VJ, (1998) Allelopathic interactions between sponges on a tropical reef. Ecology 79: 1740-1750.
59. Wishart DS, (2007) Current Progress in computational metabolomics. Briefings in Bioinformatics 8: 279-293.
60. Müller WEG, Klemt M, Thakur NL, Schröder HC, Aiello A, et al. (2004) Molecular/chemical ecology in sponges: evidence for an adaptive antibacterial response in Suberites domuncula. Marine Biology 144: 19-29.
61. Steel HC, Cockeran R, Anderson R, (2002) Platelet-activating factor and lyso-PAF possess direct antimicrobial properties in vitro. Apmis 110: 158-164.
62. Bolser RC, Hay ME, (1996) Are tropical plants better defended? Palatability and defenses of temperate vs tropical seaweeds. Ecology 77: 2269-2286.
63. Zabala M, Ballesteros E, (1989) Surface-dependent strategies and energy flux in benthic marine communities or why corals do not exist in the Mediterranean. Scientia Marina 53: 3-17.
64. Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M, et al. (2002) Molecular Evidence for a Uniform Microbial Community in Sponges from Different Oceans. Applied and Environmental Microbiology 68: 4431-4440.
65. Mohamed NM, Enticknap JJ, Lohr JE, Mcintosh SM, Hill RT, (2008) Changes in bacterial communities of the marine sponge Mycale laxissima on transfer into aquaculture. Applied Environmental Microbiology 74: 1209-1222.
66. Friedrich AB, Fischer I, Proksch P, Hacker J, Hentschel U, (2001) Temporal variation of the microbial community associated with the Mediterranean sponge Aplysina aerophoba. FEMS Microbiology Ecology 38: 105-113.
67. Taylor MW, Schupp PJ, de Nys R, Kjelleberg S, Steinberg PD, (2005) Biogeography of bacteria associated with the marine sponge Cymbastela concentrica. Environmental Microbiology 7: 419-433.