New Class of Blue Animal Pigments Based on Frizzled and Kringle Protein Domains

Abstract

The nature of coloration in many marine animals remains poorly investigated. Here we studied the blue pigment of a scyfoid jellyfish Rhizostoma pulmo and determined it to be a soluble extracellular 30-kDa chromoprotein with a complex absorption spectrum peaking at 420, 588, and 624 nm. Furthermore, we cloned the corresponding cDNA and confirmed its identity by immunoblotting and mass spectrometry experiments. The chromoprotein, named rpulFKz1, consists of two domains, a Frizzled cysteine-rich domain and a Kringle domain, inserted into one another. Generally, Frizzleds are members of a basic Wnt signal transduction pathway investigated intensely with regard to development and cancerogenesis. Kringles are autonomous structural domains found throughout the blood clotting and fibrinolytic proteins. Neither Frizzled and Kringle domains association with any type of coloration nor Kringle intrusion into Frizzled sequence was ever observed. Thus, rpulFKz1 represents a new class of animal pigments, whose chromogenic group remains undetermined. The striking homology between a chromoprotein and members of the signal transduction pathway provides a novel node in the evolution track of growth factor-mediated morphogenesis compounds.Pigments in nature play important roles ranging from camouflage coloration and sunscreen to visual reception and participation in biochemical pathways (1). Considering the spectral diversity of pigment-based coloration in animals one can conclude that blue pigments occur relatively rare (as a rule blue coloration results from light diffraction or scattering rather than the presence of a blue pigment). At least partially this fact is explained by an inevitably more complex structure of blue pigments compared to yellow-reds. To appear blue a compound must contain an extended and usually highly polarized system of the conjugated -electrons.In many organisms blue coloration is achieved by combining a chromophore with a specific apoprotein, which organizes the chromophore and provides red-shift upon binding. For example, carotenoprotein crustacyanin, a well studied blue pigment from the lobster shell, contains orange carotenoid astaxanthin, which demonstrates a strong bathochromic shift due to noncovalent binding to a protein of lipocalin family (2).Several known types of protein-based animal pigments can be distinguished: carotenoproteins (including rhodopsins, where carotenoids feature an unusual covalent bond to apoprotein), heme-, flavin-, or metal-containing proteins, pterins, melanins, ommochromes (1), and members of the green fluorescent protein (GFP) 1 family (3). Each type is characterized by specific chromogenic groups and protein sequences.In the present work we studied the blue pigment of the scyfoid jellyfish Rhizostoma pulmo. We anticipated to find either a carotenoprotein (being the most widely spread pigment class (1)) or GFP-like chromoprotein (as many fluorescent and colored GFP-like proteins were found earlier in Cnidaria (3)). However, this work revealed a new class of pigments base...

Rhizostomins: A Novel Pigment Family From Rhizostome Jellyfish (Cnidaria, Scyphozoa)

“…Our search demonstrated that Fz-CRD and KR domains are ubiquitous among cnidarians, yet only eight protein sequences were discovered that fall within the same clade and have the same domain structure as rpulFKz1 (Bulina et al, 2004). Among these proteins, the sequence that belongs to Cassiopea xamachana has motifs that mostly match Cassio Blue tryptic digests (Phelan et al, 2006).…”

Taxonomic and functional diversity increase the aesthetic value of coralligenous reefs

“…This may be explained by their low coverages in the photos (coverages of 0.2% for green, and 0.5% for blue). Indeed, within the circalittoral shelf, where coralligenous reefs grow, chlorophyll organisms (including green algae) are less abundant because of a lack of light, and blue pigments are relatively rare in animal colouration 35 .…”

On the perception, production and function of blue colouration in animals

“…The colour literature contains a large body of work on the physics and chemistry of colour production and blue colours have received considerable research attention (Goodrich & Reisinger, 1953;Dyck, 1971;Veron, 1973;Rohrlich, 1974;Byers, 1975;Filshie, Day & Mercer, 1975;Kazlauskas et al, 1982;Blanquet & Phelan, 1987;Wilson, 1987;Goda & Fujii, 1995Brink & Lee, 1999;Vukusic et al, 2001;Kinoshita, Yoshioka & Kawagoe, 2002;Bulina et al, 2004;Vukusic & Hooper, 2005;Watanabe et al, 2005;Doucet et al, 2006;Bagnara, Fernandez & Fujii, 2007;Simmonis & Berthier, 2012). This research attention may reflect our curiosity about brilliantly blue-coloured animals and the potential that colourproducing mechanisms have for biomimetic industrial applications.…”

“…carotenoids), but blue pigments are rare, perhaps because they necessitate more complex chemistry. For example, the blue pigment compound of the bryozoan Rhizostoma pulmo requires a very long and highly polarized chain of single-double alternating carbon bonds (Bulina et al, 2004). When they are present blue pigments are more likely to be found in the extracellular matrix for example in the copepod Pontella fera, the crayfish Procambarus clarkii and the abalone Haliotis discus hannai (Herring, 1965;Cheesman, Lee & Zagalsky, 1967;Milicua et al, 1985).…”