Colorful seashells: Identification of haem pathway genes associated with the synthesis of porphyrin shell color in marine snails

Abstract

Very little is known about the evolution of molluskan shell pigments, although Mollusca is a highly diverse, species rich, and ecologically important group of animals comprised of many brightly colored taxa. The marine snail genus Clanculus was chosen as an exceptional model for studying the evolution of shell color, first, because in Clanculus margaritarius and Clanculus pharaonius both shell and foot share similar colors and patterns; and second, because recent studies have identified the pigments, trochopuniceus (pink‐red), and trochoxouthos (yellow‐brown), both comprised of uroporphyrin I and uroporphyrin III, in both shell and colored foot tissue of these species. These unusual characteristics provide a rare opportunity to identify the genes involved in color production because, as the same pigments occur in the shell and colored foot tissue, the same color‐related genes may be simultaneously expressed in both mantle (which produces the shell) and foot tissue. In this study, the transcriptomes of these two Clanculus species along with a third species, Calliostoma zizyphinum, were sequenced to identify genes associated with the synthesis of porphyrins. Calliostoma zizyphinum was selected as a negative control as trochopuniceus and trochoxouthos were not found to occur in this species. As expected, genes necessary for the production of uroporphyrin I and III were found in all three species, but gene expression levels were consistent with synthesis of uroporphyrins in mantle and colored foot tissue only in Clanculus. These results are relevant not only to understanding the evolution of shell pigmentation in Clanculus but also to understanding the evolution of color in other species with uroporphyrin pigmentation, including (mainly marine) mollusks soft tissues and shells, annelid and platyhelminth worms, and some bird feathers.

High-resolution linkage and quantitative trait locus mapping using an interspecific cross between Argopecten irradians irradians (♀) and A. purpuratus (♂)

“…Studies have revealed that uroporphyrin pigments are responsible for coloration of shells and soft tissues in several molluscs (reviewed in Williams 2017). In scallops and marine snails, several genes related to porphyrin metabolism were differentially expressed in mantles with different colors (Ding et al 2015;Williams et al 2017), whereas for MECOM, the difference is not significant in adult mantle tissues suggesting that it may express and function during early shell formation. In this study, the QTLs related to shell coloration and growth were revealed by mapping with one bi-parental family, which represents only a small cross section of the breeding germplasm.…”

Chemical evidence of rare porphyrins in purple shells of Crassostrea gigas oyster

“…As recently demonstrated in the case of marine snail, carboxylic acid porphyrins contribute to the pink-red and yellow-brown colours of shells 20 . These porphyrins are considered as side products of the haem biosynthetic pathway 3 . Haem is a well-known porphyrin complexed with Fe(II), able to transport oxygen indispensable for cellular aerobic respiration.…”

“…This gap of knowledge is partly due to the lack of elucidation of the chemical nature of shell pigments, particularly in the Crassostrea genus. By combining the identification of shell pigments with corresponding biosynthetic pathways and associated genes, key information on the relation between shell colouration, mineralization or other molecular mechanisms can be obtained as previously reported in marine snails 3 . Therefore, the identification of shell pigments appears to be a possible gateway to the recovery of natural dyes from wasted oyster shells for a broad range of applications in health or material science, helping to contribute to a sustainable future for shellfish farming industry 1 .…”

Comparative transcriptomic and proteomic analysis of yellow shell and black shell pearl oysters, Pinctada fucata martensii

“…Another study showed that the notch signalling pathway plays a vital role in shell pigmentation in the clam Meretrix meretrix , while calcium signalling may activate this pathway and influence shell colour [12]. Sequential layer-by-layer mineralisation is directed by cells of the mantle edge in Pfu ., and pigments, glycoproteins and polysaccharides in the periostracum layer are secreted by the mantle or foot tissue in molluscs [13, 14]. Thus, there may be a close relationship between biomineralisation and pigment deposition, with some genes acting as a bridge between these two biological phenomena.…”