marine drugs Article
How Environmental Factors Affect the Production of Guanidine Alkaloids by the Mediterranean Sponge Crambe crambe Eva Ternon 1, *, Erica Perino 2 , Renata Manconi 3 , Roberto Pronzato 2 and Olivier P. Thomas 1,4, * 1 2 3 4
*
Université Côte d’Azur, CNRS, OCA, IRD, Géoazur, 250 rue Albert Einstein, 06560 Valbonne, France Dipartimento di Scienze della Terra, dell’Ambiente e della Vita, Università di Genova, Corso Europa 26, 16132 Genoa, Italy; [email protected] (E.P.); [email protected] (R.P.) Dipartimento di Scienze della Natura e del Territorio, Università di Sassari, Via Muroni 25, 07100 Sassari, Italy; [email protected] Marine Biodiscovery, School of Chemistry, National University of Ireland Galway, University Road, H91 TK33 Galway, Ireland Correspondence: [email protected] (E.T.); [email protected] (O.P.T.); Tel.: +353-(0)91493563 (O.P.T.)
Academic Editor: Paul Long Received: 6 December 2016; Accepted: 12 June 2017; Published: 16 June 2017
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. Keywords: sponge; abiotic factors; specialized metabolome; metabolomics; sponge farming
1. Introduction Marine sponges are known to produce a large array of small molecules also called specialized metabolites that are likely to be involved in allelopathic interactions [1–6]. From a biotechnological point of view, such metabolites are frequently investigated, mostly for pharmaceutical applications [7–9]. Several biotechnological approaches have been developed for the large-scale production of these high value-added marine products which include in situ and ex situ farming, primmorph or cell culture [10,11]. Farming explants in situ has been considered as one of the most cost-effective ways to guarantee sufficient sustainable bioactive metabolites [12]. Since spatial and temporal variations in concentrations of major specialized metabolites have been documented previously [13–15], the ideal farming location that promotes their biosynthesis as well as the harvest season have to be assessed. Mar. Drugs 2017, 15, 181; doi:10.3390/md15060181
www.mdpi.com/journal/marinedrugs
Mar. Drugs 2017, 15, 181
2 of 15
The natural variations in the production of the specialized metabolites have been mostly explained by environmental and ecological factors like biotic interactions [16–19], abiotic factors [13,20–22] or more rarely, the organism’s life cycle [15,23] as well as physiological state [24,25]. Overall, the effects of abiotic factors on the production of specialized metabolites have produced contrasting results so far [20,26–29]. As highly effective filter feeders, marine sponges are able to take up a large range (
How Environmental Factors Affect the Production of Guanidine Alkaloids by the Mediterranean Sponge Crambe crambe Eva Ternon 1, *, Erica Perino 2 , Renata Manconi 3 , Roberto Pronzato 2 and Olivier P. Thomas 1,4, * 1 2 3 4
*
Université Côte d’Azur, CNRS, OCA, IRD, Géoazur, 250 rue Albert Einstein, 06560 Valbonne, France Dipartimento di Scienze della Terra, dell’Ambiente e della Vita, Università di Genova, Corso Europa 26, 16132 Genoa, Italy; [email protected] (E.P.); [email protected] (R.P.) Dipartimento di Scienze della Natura e del Territorio, Università di Sassari, Via Muroni 25, 07100 Sassari, Italy; [email protected] Marine Biodiscovery, School of Chemistry, National University of Ireland Galway, University Road, H91 TK33 Galway, Ireland Correspondence: [email protected] (E.T.); [email protected] (O.P.T.); Tel.: +353-(0)91493563 (O.P.T.)
Academic Editor: Paul Long Received: 6 December 2016; Accepted: 12 June 2017; Published: 16 June 2017
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. Keywords: sponge; abiotic factors; specialized metabolome; metabolomics; sponge farming
1. Introduction Marine sponges are known to produce a large array of small molecules also called specialized metabolites that are likely to be involved in allelopathic interactions [1–6]. From a biotechnological point of view, such metabolites are frequently investigated, mostly for pharmaceutical applications [7–9]. Several biotechnological approaches have been developed for the large-scale production of these high value-added marine products which include in situ and ex situ farming, primmorph or cell culture [10,11]. Farming explants in situ has been considered as one of the most cost-effective ways to guarantee sufficient sustainable bioactive metabolites [12]. Since spatial and temporal variations in concentrations of major specialized metabolites have been documented previously [13–15], the ideal farming location that promotes their biosynthesis as well as the harvest season have to be assessed. Mar. Drugs 2017, 15, 181; doi:10.3390/md15060181
www.mdpi.com/journal/marinedrugs
Mar. Drugs 2017, 15, 181
2 of 15
The natural variations in the production of the specialized metabolites have been mostly explained by environmental and ecological factors like biotic interactions [16–19], abiotic factors [13,20–22] or more rarely, the organism’s life cycle [15,23] as well as physiological state [24,25]. Overall, the effects of abiotic factors on the production of specialized metabolites have produced contrasting results so far [20,26–29]. As highly effective filter feeders, marine sponges are able to take up a large range (
