How Environmental Factors Affect the Production of Guanidine Alkaloids by the Mediterranean Sponge Crambe crambe

Abstract

Most marine sponges are known to produce a large array of low molecular-weight metabolites which have applications in the pharmaceutical industry. The production of so-called specialized metabolites may be closely related to environmental factors. In this context, assessing the contribution of factors like temperature, nutrients or light to the metabolomes of sponges provides relevant insights into their chemical ecology as well as the supply issue of natural sponge products. The sponge Crambe crambe was chosen as a model due to its high content of specialized metabolites belonging to polycyclic guanidine alkaloids (PGA). First results were obtained with field data of both wild and farmed specimens collected in two seasons and geographic areas of the North-Western Mediterranean. Then, further insights into factors responsible for changes in the metabolism were gained with sponges cultivated under controlled conditions in an aquarium. Comparative metabolomics showed a clear influence of the seasons and to a lesser extent of the geography while no effect of depth or farming was observed. Interestingly, sponge farming did not limit the production of PGA, while ex situ experiments did not show significant effects of several abiotic factors on the specialized metabolome at a one-month time scale. Some hypotheses were finally proposed to explain the very limited variations of PGA in C. crambe placed under different environmental conditions.

Marine natural products

“…Conversely, seasonal effects were apparent. 521 An independent detailed investigation of the absolute conguration of aurantosides G and J using computational approaches has validated the results suggested by total synthesis. 522 A metagenomic analysis of the microbial community associated with the chemically prolic sponge Theonella swinhoei has identied a new pathway to the keramamides, sponge-derived peptides containing the rare halohydroxytryptophan motif.…”

Metabolome variability for two Mediterranean sponge species of the genus Haliclona: specificity, time, and space

“…There is still a debate whether changing environmental conditions such as temperature produces variations in the production of specialized metabolites. Several studies have found higher concentrations of specialized metabolites in summer corresponding to maximum yearly temperatures (Abdo et al 2007;Ternon et al 2017;De Caralt et al 2013) while other studies failed to find seasonal changes in production of metabolites (Duckworth et al 2012;López-Legentil et al 2006). In this study, a clear decrease of specialized metabolites occurred in April and May, when temperature in the Northwestern Mediterranean starts to increase after winter (http://somlit.mio.univ-amu.fr), but no further variation occurred during the warmest period (August-October), indicating the fluctuation in the metabolomes might be due to sponge physiological responses rather than environmental parameters.…”

“…In the marine environment, spatial and temporal variations of specialized metabolites have been studied in algae (Payo et al 2011;Soares et al 2015), cnidarians (Kelman et al 2000;He et al 2014;Costa-Lotufo et al 2018), tunicates (López-Legentil et al 2006), bryozoans (Peters et al 2004) and sponges (Reverter et al 2016;Ternon et al 2017;Sacristan-Soriano et al 2011). Spatial variation of metabolites has been mostly related to local adaptation to the environment and fluctuating parameters such as temperature, light, or chlorophyll concentrations.…”

“…In a recent study, Soares et al (2015) found different chemotypes of the brown alga Stypopodium zonale in different geographic locations, probably indicative of genotypic sorting across habitats. Seasonal changes of specialized metabolites possibly related to changes of environmental parameters such as temperature have been observed in some marine invertebrates (Page et al 2005;Sacristán-Soriano et al 2012;Ternon et al 2017). According to the optimal defence theory (ODT) (Rhoades 1985), the energy allocated to the biosynthesis of specialized metabolites results from the continual trade-off with the energy invested in primary functions such as growth and reproduction.…”

The Investigation of the Ball Sponge <i>Cinachyrella kuekenthali</i> from Two Different Environments on Jamaica’s North Coast

“…An example of a study of a sponge species which did not differ in metabolite concentration is that of the sponge Crambe crambe which was collected from different geographical regions in the Mediterranean (Liguarian Sea and Sardinia Sea) and examined for the occurrence of crambescidins and crambescins [21].…”