Molecular Pathways and Pigments Underlying the Colors of the Pearl Oyster Pinctada margaritifera var. cumingii (Linnaeus 1758)

Abstract

The shell color of the Mollusca has attracted naturalists and collectors for hundreds of years, while the molecular pathways regulating pigment production and the pigments themselves remain poorly described. In this study, our aim was to identify the main pigments and their molecular pathways in the pearl oyster Pinctada margaritifera—the species displaying the broadest range of colors. Three inner shell colors were investigated—red, yellow, and green. To maximize phenotypic homogeneity, a controlled population approach combined with common garden conditioning was used. Comparative analysis of transcriptomes (RNA-seq) of P. margaritifera with different shell colors revealed the central role of the heme pathway, which is involved in the production of red (uroporphyrin and derivates), yellow (bilirubin), and green (biliverdin and cobalamin forms) pigments. In addition, the Raper–Mason, and purine metabolism pathways were shown to produce yellow pigments (pheomelanin and xanthine) and the black pigment eumelanin. The presence of these pigments in pigmented shell was validated by Raman spectroscopy. This method also highlighted that all the identified pathways and pigments are expressed ubiquitously and that the dominant color of the shell is due to the preferential expression of one pathway compared with another. These pathways could likely be extrapolated to many other organisms presenting broad chromatic variation.

Identifying genes associated with genetic control of color polymorphism in the pearl oysterPinctada margaritiferavar.cumingii(Linnaeus 1758) using a comparative whole genome pool‐sequencing approach

“…The red specific SNPs showed functional enrichment for hydroxymethylbilane synthase activity (GO:0004418), a pathway containing the gene porphobilinogen deaminase (PBGD). This GO category was already identified as specific to the red color in a previous study (Stenger et al, 2021a), in which PBGD was significantly downregulated in the red phenotype compared to the yellow and green phenotypes. This downregulation causes a form of acute intermittent porphyria (AIP) in mammals, linked with the accumulation of uroporphyrin I in cells, a well-known red pigment that was previously identified in marine bivalve shells (Stenger et al, 2021a).…”

“…This GO category was already identified as specific to the red color in a previous study (Stenger et al, 2021a), in which PBGD was significantly downregulated in the red phenotype compared to the yellow and green phenotypes. This downregulation causes a form of acute intermittent porphyria (AIP) in mammals, linked with the accumulation of uroporphyrin I in cells, a well-known red pigment that was previously identified in marine bivalve shells (Stenger et al, 2021a). This kind of porphyria may here be the result of a non-functional PBGD protein due to a SNP (Balwani & Desnick, 2012;Meyer et al, 1972;Schneider-Yin et al, 2002;Siersema et al, 1990;Song et al, 2009).…”

Identification of a coproporphyrinogen-III oxidase gene and its correlation with nacre color in Hyriopsis cumingii

“…CPOX is an indispensable enzyme that is required for the synthesis of heme in different organisms. Some studies found that many different pigments (e.g., uroporphyrin, cobalamin, phorcabilin, biliverdin, and bilirubin) are produced in the synthesis and decomposition pathways of heme, which affect the shell color in Pinctada margaritifera [ 31 ]. If the heme synthesis pathway is affected, it may also lead to the formation of different shell colors in marine snails [ 20 ].…”

First Evidence of Ommochromes in Bivalves: the Case of the Edible Oyster Crassostrea Gigas

“…Coloured molecules are also poorly described due to their low content in the shell and the di culty of their selective extraction from the calcareous material. While the presence of few tetrapyrroles, such as uroporphyrin and biliverdin, are now well established [2][3][4] , the occurrence of melanins in shells of bivalves is apparently less common than generally expected, as illustrated by the recent work of S. Affenzeller et al 5 . For instance, the black colour of the adductor muscle scar of shells of the edible oyster Crassostrea gigas, initially hypothesized as a contribution of melanins by S. Hao et al 6 , was subsequently ruled out without resolving the nature of this colour.…”