Biochemical Trade-Offs: Evidence for Ecologically Linked Secondary Metabolism of the Sponge Oscarella balibaloi

et al. (2011) Biochemical Trade-Offs: Evidence for Ecologically Linked Secondary Metabolism of the Sponge Oscarella balibaloi. PLoS ONE 6(11): e28059. doi:10.1371/journal.pone.0028059 Biochemical Trade-Offs: Evidence for Ecologically Linked Secondary Metabolism of the Sponge Oscarella balibaloi Julijana Ivanisevic 0 Olivier P. Thomas 0 Laura Pedel 0 Nicolas Pe nez 0 Alexander V. Ereskovsky 0 Ge rald 0 Culioli 0 Thierry Pe rez 0 Jonathan H. Badger, J. Craig Venter Institute, United States of America 0 1 Universite de la Me diterrane e, Centre d'Oce anologie de Marseille, Aix-Marseille Universite , CNRS UMR 6540 DIMAR, Station Marine d'Endoume , Marseille , France , 2 Universite de Nice-Sophia Antipolis, Laboratoire de Chimie des Mole cules Bioactives et des Aro mes, CNRS UMR 6001, Institut de Chimie de Nice , Parc Valrose, Nice , France , 3 Universite du Sud Toulon-Var, Laboratoire MAPIEM , EA 4323, La Garde , France Secondary metabolite production is assumed to be costly and therefore the resource allocation to their production should be optimized with respect to primary biological functions such as growth or reproduction. Sponges are known to produce a great diversity of secondary metabolites with powerful biological activities that may explain their domination in some hard substrate communities both in terms of diversity and biomass. Oscarella balibaloi (Homoscleromorpha) is a recently described, highly dynamic species, which often overgrows other sessile marine invertebrates. Bioactivity measurements (standardized Microtox assay) and metabolic fingerprints were used as indicators of the baseline variations of the O. balibaloi secondary metabolism, and related to the sponge reproductive effort over two years. The bioactivity showed a significant seasonal variation with the lowest values at the end of spring and in early summer followed by the highest bioactivity in the late summer and autumn. An effect of the seawater temperature was detected, with a significantly higher bioactivity in warm conditions. There was also a tendency of a higher bioactivity when O. balibaloi was found overgrowing other sponge species. Metabolic fingerprints revealed the existence of three principal metabolic phenotypes: phenotype 1 exhibited by a majority of low bioactive, female individuals, whereas phenotypes 2 and 3 correspond to a majority of highly bioactive, non-reproductive individuals. The bioactivity was negatively correlated to the reproductive effort, minimal bioactivities coinciding with the period of embryogenesis and larval development. Our results fit the Optimal Defense Theory with an investment in the reproduction mainly shaping the secondary metabolism variability, and a less pronounced influence of other biotic (species interaction) and abiotic (temperature) factors. - Funding: This work was supported by the ECIMAR program (ANR-06-BDIV-001-04) and European Marie Curie Mobility program (MIF1-CT-2006-040065). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Secondary metabolites have important ecological functions, acting as key mediators in the interaction between organisms and their environment. Their antipredatory and allelopathic roles were exhaustively studied in plant-herbivore and plant-plant interactions [1], whereas their contribution to the functioning of marine biological systems remains poorly explored. However the use of chemical cues is commonplace in marine benthic invertebrates, especially in sessile filter-feeders which are subject to high environmental pressures such as predation, fouling and competition for space and feeding resources [2,3]. Considering the fact that primary and secondary metabolites have the same chemical precursors (substrates, cofactors), their respective biosynthesis are generally considered to result from a costly trade-off at the biochemical level [4,5,6]. Thus, the energy allocated to the secondary metabolism, which mainly dedicated to chemical defenses, is subtracted from the amount of resources available to the remaining physiological functions. Assuming the high cost associated with the production, transport and storage of secondary metabolites, several concepts explaining their evolution and selection have been developed for terrestrial plants and applied to marine organisms. One of the best known models of energy allocation for the production of secondary metabolites is the Optimal Defense Theory (ODT). The ODT asserts that organisms allocate resources to chemical defenses in a way that maximizes fitness [4,6] and preserves the primary biological functions such as homeostasis maintenance, growth and reproduction. Primary biological functions are mostly determined by seasonal fluctuations of some environmental parameters [7]. Therefore the natural toxicity of an organism and the production of secondary metabolites should vary as a result of a trade-off with primary biological functions, or as a response to biotic and abiotic environmental parameters [8,9,10,11,12,13]. Measurements of the bioactivity were often used as indicators in order to determine the baseline variations of the secondary metabolism [13,14]. Spatial and temporal variations of bioactivity and concentrations of some secondary metabolites were already documented in few sponges, ascidians, and other sessile marine invertebrates [9,15,16,17,18,19]. Natural variations were mostly explained by ecological and environmental factors, like biotic interactions [20,21,22,23], habitat type, temperature, depth or salinity [15,16,18,24,25,26], whereas the link with the organisms life cycle (growth, reproduction) or its physiological state was rarely investigated [2,9,18,27,28]. Regarding secondary metabolites themselves, only few target metabolites were generally studied owing to their valorisation potential, whereas a more holistic view of the metabolome of an organism was not investigated until recently. The tools to carry out such substantial studies have only recently been accessible in a cost effective sense. Metabolomic approaches can be valuable tools in ecophysiology and ecotoxicology to characterize the physiological responses of an organism at the molecular level, or to learn about the state or condition of the environment (environmental metabolomics and chemical risk assessment) [29,30]. These approaches are based on a broader metabolome investigation and can provide useful biomarkers of the organisms health and highlight compounds involved in physiological processes or ecological interactions [31]. Sponges produce a great diversity of secondary metabolites, with original biosynthetic pathways and biological activities [32]. These chemical weapons may explain their dominance in some hard substrate communities both in terms of diversity and biomass [33]. This is especially the case in Mediter (...truncated)