Differential Expression of the Demosponge (Suberites domuncula) Carotenoid Oxygenases in Response to Light: Protection Mechanism Against the Self-Produced Toxic Protein (Suberitine)

Abstract

Abstract:The demosponge Suberites domuncula has been described to contain high levels of a proteinaceous toxin, Suberitine, that displays haemolytic activityIn the present study this 7-8 kDa polypeptide has been isolated and was shown to exhibit also cytotoxic effects on cells of the same species. Addition of retinal, a recently identified metabolite of β-carotene that is abundantly present in S. domuncula was found to reduce both the haemolytic and the cell toxic activity of Suberitine at a molar ratio of 1:1. Spectroscopic analyses revealed that the interaction between β-carotene and Suberitine can be ascribed to a reversible energy transfer reaction. The enzyme that synthesises retinal in the sponge system is the β,β-carotene-15,15′-dioxygenase [carotene dioxygenase]. In order to clarify if this enzyme is the only β-carotene-metabolizing enzyme a further oxygenase had been identified and cloned, the (related) carotenoid oxygenase. In contrast to the dioxygenase, the carotenoid oxygenase could not degrade β-carotene or lycopene in Escherichia coli strains that produced these two carotenoids; therefore it had been termed related-carotenoid oxygenase. Exposure of primmorphs to light of different wavelengths from the visible OPEN ACCESSMar. Drugs 2012, 10 178 spectrum resulted after 3 days in a strong upregulation of the dioxygenase in those 3D-cell aggregates that had been incubated with β-carotene. The strongest effect is seen with blue light at a maximum around 490 nm. It is concluded that the toxin Suberitine is non-covalently modified by retinal, the cleavage product from β-carotene via the enzyme carotene dioxygenase, a light inducible oxygenase. Hence, this study highlights that in S. domuncula the bioactive metabolite, retinal, has the property to detoxify its homologous toxin.

Palmitoylation of Metazoan Carotenoid Oxygenases

“…It is of interest to note that Mortierella verticillata, a fungus harboring an ACOL ( Figure 6; along with a sister species M. elongata), has been shown to be a recipient of HGT [30], while sponges and cnidarians, and other early diverging metazoans, have been the subject of much interest in this area [31,32]. Two proteins from this subfamily were previously described in sponges (Suberites domuncula) and were found to have no β-carotene or lycopene cleavage activity in carotenoid producing E. coli [28].…”

“…This suggests that functional changes of ACOL compared to apocarotenoid oxygenases (ACO) are unlikely although results of the test should be treated with a caution (see the "Methods" section). Still, a plausible explanation is that the function of ACOL is likely to be the same or similar to cyanobacterial homologs consistent with lack of activity towards a full length carotenoids [28]. for the heuristic search were obtained automatically by applying Neighbor-Join and BioNJ algorithms to a matrix of pairwise distances estimated using a WAG (Whelan-and-Goldman) model, and then selecting the topology with superior log likelihood value.…”

Elements of a ‘nervous system’ in sponges

“…Therefore, this animal would most likely have evolved in shallow waters in competition with other flagellates and have specialized to be efficient at filtering. (Müller et al, 2012).…”

Novel natural product discovery from obligate symbiotic organisms of marine sponges

“…In addition, acetylenic carotenoid sulfates termed bastaxanthins, and other related compounds thought to be fucoxanthin metabolites derived from microalgae [69] , have been isolated from the marine sponges Ianthella basta [52] and Prianos osiros [70] . Recent molecular studies aimed at elucidating the main elements of the retinoid metabolic pathway in the demosponge S. domuncula revealed that the retinoid precursor b-carotene, which is enzymatically cleaved via the enzyme b-b-carotene 15,15'-dioxygenease to generate retinal, is generated by bacteria that form a symbiotic association with this sponge [71,72] .…”