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Mass spectrometry imaging reveals new biological roles for choline esters and Tyrian purple precursors in muricid molluscs.

Rudd D, Ronci M, Johnston MR, Guinan T, Voelcker NH, Benkendorff K - Sci Rep (2015)

Bottom Line: But during egg-laying, murexine was transferred to the capsule gland, and then to the egg capsules, where chemical ripening resulted in Tyrian purple formation.Murexine was found to tranquilise the larvae and may relax the reproductive tract.This study shows that DIOS-MSI is a powerful tool that can provide new insights into marine chemo-ecology.

View Article: PubMed Central - PubMed

Affiliation: School of Biological Sciences, Flinders University, Bedford Park, SA 5042, Australia.

ABSTRACT
Despite significant advances in chemical ecology, the biodistribution, temporal changes and ecological function of most marine secondary metabolites remain unknown. One such example is the association between choline esters and Tyrian purple precursors in muricid molluscs. Mass spectrometry imaging (MSI) on nano-structured surfaces has emerged as a sophisticated platform for spatial analysis of low molecular mass metabolites in heterogeneous tissues, ideal for low abundant secondary metabolites. Here we applied desorption-ionisation on porous silicon (DIOS) to examine in situ changes in biodistribution over the reproductive cycle. DIOS-MSI showed muscle-relaxing choline ester murexine to co-localise with tyrindoxyl sulfate in the biosynthetic hypobranchial glands. But during egg-laying, murexine was transferred to the capsule gland, and then to the egg capsules, where chemical ripening resulted in Tyrian purple formation. Murexine was found to tranquilise the larvae and may relax the reproductive tract. This study shows that DIOS-MSI is a powerful tool that can provide new insights into marine chemo-ecology.

No MeSH data available.


Related in: MedlinePlus

The proposed biological role of murexine in the D. orbita egg capsules using a larval motility assay in the presence of 50 ppm murexine extract:(a) percentage of motile larvae counted using short 30 s videos over 60 min and (b) a video still shot of larvae at time 0 prior to the addition of murexine extract (video online: https://youtu.be/rlCvyyhnXAE).
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f6: The proposed biological role of murexine in the D. orbita egg capsules using a larval motility assay in the presence of 50 ppm murexine extract:(a) percentage of motile larvae counted using short 30 s videos over 60 min and (b) a video still shot of larvae at time 0 prior to the addition of murexine extract (video online: https://youtu.be/rlCvyyhnXAE).

Mentions: The role of murexine within the egg capsules as a natural tranquiliser during larval development is also plausible. To test this, we purified murexine at 0.22 mM (50 mg/L) and confirmed that it has a temporary tranquilising effect on late stage intracapsular larvae lasting over 60 minutes (Fig. 6a and Supplementary Video 1). Developing larvae shells are delicate and oxygen is limited during muricid intracapsular development46, despite this period being a metabolically active period. D. orbita reproductive females could be provisioning offspring with intracapsular tranquilisers to ensure they develop ready for life in the open sea. Indeed nearly 100% hatching success rate has been reported for the thousands of delicate larvae contained within each egg capsule of D. orbita47. Natural tranquilisers have been previously reported in molluscan egg masses, specifically in the common squid Loligo vulgaris, which incorporates an unidentified natural tranquiliser in perivitalline fluid within egg cases48, preventing premature hatching. Although the bioactive compound in squid perivitalline fluid does not appear to have been identified to date, cephalopods do not possess a hypobranchial gland and there are no reports of choline esters in the venom glands, ink or chemical messengers involved in the reproduction of cephalopods, despite extensive studies344950. Therefore, the new biological role proposed here for murexine, appears to be an interesting example of functional convergent evolution between the gastropods and cephalopods. These two classes of marine molluscs have independantly evolved the deposition of benthic masses, as well as chemical sedatives to protect the encapsulated larvae.


Mass spectrometry imaging reveals new biological roles for choline esters and Tyrian purple precursors in muricid molluscs.

Rudd D, Ronci M, Johnston MR, Guinan T, Voelcker NH, Benkendorff K - Sci Rep (2015)

The proposed biological role of murexine in the D. orbita egg capsules using a larval motility assay in the presence of 50 ppm murexine extract:(a) percentage of motile larvae counted using short 30 s videos over 60 min and (b) a video still shot of larvae at time 0 prior to the addition of murexine extract (video online: https://youtu.be/rlCvyyhnXAE).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4555103&req=5

f6: The proposed biological role of murexine in the D. orbita egg capsules using a larval motility assay in the presence of 50 ppm murexine extract:(a) percentage of motile larvae counted using short 30 s videos over 60 min and (b) a video still shot of larvae at time 0 prior to the addition of murexine extract (video online: https://youtu.be/rlCvyyhnXAE).
Mentions: The role of murexine within the egg capsules as a natural tranquiliser during larval development is also plausible. To test this, we purified murexine at 0.22 mM (50 mg/L) and confirmed that it has a temporary tranquilising effect on late stage intracapsular larvae lasting over 60 minutes (Fig. 6a and Supplementary Video 1). Developing larvae shells are delicate and oxygen is limited during muricid intracapsular development46, despite this period being a metabolically active period. D. orbita reproductive females could be provisioning offspring with intracapsular tranquilisers to ensure they develop ready for life in the open sea. Indeed nearly 100% hatching success rate has been reported for the thousands of delicate larvae contained within each egg capsule of D. orbita47. Natural tranquilisers have been previously reported in molluscan egg masses, specifically in the common squid Loligo vulgaris, which incorporates an unidentified natural tranquiliser in perivitalline fluid within egg cases48, preventing premature hatching. Although the bioactive compound in squid perivitalline fluid does not appear to have been identified to date, cephalopods do not possess a hypobranchial gland and there are no reports of choline esters in the venom glands, ink or chemical messengers involved in the reproduction of cephalopods, despite extensive studies344950. Therefore, the new biological role proposed here for murexine, appears to be an interesting example of functional convergent evolution between the gastropods and cephalopods. These two classes of marine molluscs have independantly evolved the deposition of benthic masses, as well as chemical sedatives to protect the encapsulated larvae.

Bottom Line: But during egg-laying, murexine was transferred to the capsule gland, and then to the egg capsules, where chemical ripening resulted in Tyrian purple formation.Murexine was found to tranquilise the larvae and may relax the reproductive tract.This study shows that DIOS-MSI is a powerful tool that can provide new insights into marine chemo-ecology.

View Article: PubMed Central - PubMed

Affiliation: School of Biological Sciences, Flinders University, Bedford Park, SA 5042, Australia.

ABSTRACT
Despite significant advances in chemical ecology, the biodistribution, temporal changes and ecological function of most marine secondary metabolites remain unknown. One such example is the association between choline esters and Tyrian purple precursors in muricid molluscs. Mass spectrometry imaging (MSI) on nano-structured surfaces has emerged as a sophisticated platform for spatial analysis of low molecular mass metabolites in heterogeneous tissues, ideal for low abundant secondary metabolites. Here we applied desorption-ionisation on porous silicon (DIOS) to examine in situ changes in biodistribution over the reproductive cycle. DIOS-MSI showed muscle-relaxing choline ester murexine to co-localise with tyrindoxyl sulfate in the biosynthetic hypobranchial glands. But during egg-laying, murexine was transferred to the capsule gland, and then to the egg capsules, where chemical ripening resulted in Tyrian purple formation. Murexine was found to tranquilise the larvae and may relax the reproductive tract. This study shows that DIOS-MSI is a powerful tool that can provide new insights into marine chemo-ecology.

No MeSH data available.


Related in: MedlinePlus