Limits...
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

D. orbita during egg deposition and DIOS-MSI maps of egg capsules across the developmental period, in positive ion mode at 100 μm spatial resolution.(a) Reproductive adults during the encapsulation of larvae and early stage capsules adhered to substrate (photo by Rudd, D.). (b) early stage capsule sampled immediately post deposition (left panels A = whole capsule) and late stage capsule after 35 days post deposition (right panels A = encapsulated veliger larvae). DIOS-MSI of the secondary metabolites are compared to (B) scanned cross sections of the egg capsules stamped onto pSi prior to removal. Labels on the imaged regions include; embryo mass (e), intracapsular fluid, (if) and veligar (v) stage larval mass. Ion maps m/z 340 corresponds to tyrindoxyl hydrogen sulfate [M+H]+, m/z 421 to Tyrian purple [M+H]+, and m/z 224 to murexine [M]+. Scale bar set to 1 mm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC4555103&req=5

f5: D. orbita during egg deposition and DIOS-MSI maps of egg capsules across the developmental period, in positive ion mode at 100 μm spatial resolution.(a) Reproductive adults during the encapsulation of larvae and early stage capsules adhered to substrate (photo by Rudd, D.). (b) early stage capsule sampled immediately post deposition (left panels A = whole capsule) and late stage capsule after 35 days post deposition (right panels A = encapsulated veliger larvae). DIOS-MSI of the secondary metabolites are compared to (B) scanned cross sections of the egg capsules stamped onto pSi prior to removal. Labels on the imaged regions include; embryo mass (e), intracapsular fluid, (if) and veligar (v) stage larval mass. Ion maps m/z 340 corresponds to tyrindoxyl hydrogen sulfate [M+H]+, m/z 421 to Tyrian purple [M+H]+, and m/z 224 to murexine [M]+. Scale bar set to 1 mm.

Mentions: DIOS-MSI on the egg capsules (Fig. 5) confirmed that murexine is transferred from the female capsule gland into the egg capsules of D. orbita, which is the first report of murexine in Neogastropod egg capsules. DIOS-MSI detected murexine only in the intracapsular fluid surrounding the early stage embryos in freshly laid egg capsules, where it is co-localised with tyrindoxyl sulfate and some minor intermediate brominated indoles and end products (Fig. 5b). In the capsules with late stage veliger larvae, water soluble murexine was no longer detectable. Tyrindoxyl sulfate also decreased in intensity and distribution during encapsulated larval development (Fig. 5, Supplementary Fig. 7). Conversely, insoluble Tyrian purple increased in the late stage capsules but was barely present at the early stage. This provides evidence for a unique form of chemical ripening in the egg capsules19 involving two distinct classes of secondary metabolites specific to the Muricidae family of marine molluscs. The apparent high abundance of murexine relative to tyrindoxyl sulfate in breeding snails implies a naturally selected role for this compound during reproduction and early stage development, whereas tyrindoxyl sulfate could be acting as a controlled release counter ion to murexine within the egg capsules and hypobranchial gland. In this case, the formation of antimicrobial brominated indole intermediates during intracapsular development35 could be a secondary function fortuitously acquired over the course of Muricidae evolution.


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)

D. orbita during egg deposition and DIOS-MSI maps of egg capsules across the developmental period, in positive ion mode at 100 μm spatial resolution.(a) Reproductive adults during the encapsulation of larvae and early stage capsules adhered to substrate (photo by Rudd, D.). (b) early stage capsule sampled immediately post deposition (left panels A = whole capsule) and late stage capsule after 35 days post deposition (right panels A = encapsulated veliger larvae). DIOS-MSI of the secondary metabolites are compared to (B) scanned cross sections of the egg capsules stamped onto pSi prior to removal. Labels on the imaged regions include; embryo mass (e), intracapsular fluid, (if) and veligar (v) stage larval mass. Ion maps m/z 340 corresponds to tyrindoxyl hydrogen sulfate [M+H]+, m/z 421 to Tyrian purple [M+H]+, and m/z 224 to murexine [M]+. Scale bar set to 1 mm.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f5: D. orbita during egg deposition and DIOS-MSI maps of egg capsules across the developmental period, in positive ion mode at 100 μm spatial resolution.(a) Reproductive adults during the encapsulation of larvae and early stage capsules adhered to substrate (photo by Rudd, D.). (b) early stage capsule sampled immediately post deposition (left panels A = whole capsule) and late stage capsule after 35 days post deposition (right panels A = encapsulated veliger larvae). DIOS-MSI of the secondary metabolites are compared to (B) scanned cross sections of the egg capsules stamped onto pSi prior to removal. Labels on the imaged regions include; embryo mass (e), intracapsular fluid, (if) and veligar (v) stage larval mass. Ion maps m/z 340 corresponds to tyrindoxyl hydrogen sulfate [M+H]+, m/z 421 to Tyrian purple [M+H]+, and m/z 224 to murexine [M]+. Scale bar set to 1 mm.
Mentions: DIOS-MSI on the egg capsules (Fig. 5) confirmed that murexine is transferred from the female capsule gland into the egg capsules of D. orbita, which is the first report of murexine in Neogastropod egg capsules. DIOS-MSI detected murexine only in the intracapsular fluid surrounding the early stage embryos in freshly laid egg capsules, where it is co-localised with tyrindoxyl sulfate and some minor intermediate brominated indoles and end products (Fig. 5b). In the capsules with late stage veliger larvae, water soluble murexine was no longer detectable. Tyrindoxyl sulfate also decreased in intensity and distribution during encapsulated larval development (Fig. 5, Supplementary Fig. 7). Conversely, insoluble Tyrian purple increased in the late stage capsules but was barely present at the early stage. This provides evidence for a unique form of chemical ripening in the egg capsules19 involving two distinct classes of secondary metabolites specific to the Muricidae family of marine molluscs. The apparent high abundance of murexine relative to tyrindoxyl sulfate in breeding snails implies a naturally selected role for this compound during reproduction and early stage development, whereas tyrindoxyl sulfate could be acting as a controlled release counter ion to murexine within the egg capsules and hypobranchial gland. In this case, the formation of antimicrobial brominated indole intermediates during intracapsular development35 could be a secondary function fortuitously acquired over the course of Muricidae evolution.

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