Ommochromes in invertebrates: biochemistry and cell biology

Abstract

Ommochromes are widely occurring coloured molecules of invertebrates, arising from tryptophan catabolism through the so-called Tryptophan → Ommochrome pathway. They are mainly known to mediate compound eye vision, as well as reversible and irreversible colour patterning. Ommochromes might also be involved in cell homeostasis by detoxifying free tryptophan and buffering oxidative stress. These biological functions are directly linked to their unique chromophore, the phenoxazine/phenothiazine system. The most recent reviews on ommochrome biochemistry were published more than 30 years ago, since when new results on the enzymes of the ommochrome pathway, on ommochrome photochemistry as well as on their antiradical capacities have been obtained. Ommochromasomes are the organelles where ommochromes are synthesised and stored. Hence, they play an important role in mediating ommochrome functions. Ommochromasomes are part of the lysosome-related organelles (LROs) family, which includes other pigmented organelles such as vertebrate melanosomes. Ommochromasomes are unique because they are the only LRO for which a recycling process during reversible colour change has been described. Herein, we provide an update on ommochrome biochemistry, photoreactivity and antiradical capacities to explain their diversity and behaviour both in vivo and in vitro. We also highlight new biochemical techniques, such as quantum chemistry, metabolomics and crystallography, which could lead to major advances in their chemical and functional characterisation. We then focus on ommochromasome structure and formation by drawing parallels with the well-characterised melanosomes of vertebrates. The biochemical, genetic, cellular and microscopic tools that have been applied to melanosomes should provide important information on the ommochromasome life cycle. We propose LRO-based models for ommochromasome biogenesis and recycling that could be tested in the future. Using the context of insect compound eyes, we finally emphasise the importance of an integrated approach in understanding the biological functions of ommochromes.

Uncyclized xanthommatin is a key ommochrome intermediate in invertebrate coloration

“…We then purified ommochromasomes from housefly eyes by a combination of differential 486 centrifugation and ultracentrifugation, and we compared the extracted compounds with those of crude 487 extracts ( Fig 6A). The main metabolites of ommochromasomes were xanthommatin and its 488 decarboxylated form ( Fig 6D), in accordance to the function of ommochromasomes as ommochrome 489 factories (Figon and Casas, 2019). Based on the absorbance at 414 nm, decarboxylated xanthommatin 490 Regarding the precursors of ommochromes in housefly eyes, we could only detect tryptophan and 3-495 hydroxykynurenine but not the intermediary kynurenine.…”

“…Lastly, as far as we know, 606 there has been no experimental evidence for the formation of xanthommatin by condensing 3-607 hydroxykynurenine with xanthurenic acid. In conclusion, the formation of uncyclized xanthommatin by the oxidative dimerization of 3-hydroxykynurenine is likely to be the main biological route for the 609 biosynthesis of ommatins within ommochromasomes (Fig 8; The relatively recent description of decarboxylated xanthommatin in several species indicates that it is 614 a common biological ommatin (Figon and Casas, 2019). Yet, little is known about how 615 decarboxylation of ommatins proceeds in vivo.…”

“…We chose this species because it is 469 known to accumulate xanthommatin and some metabolites of the kynurenine pathway in its eyes 470 (Linzen, 1974). However, nothing is known about decarboxylated xanthommatin and uncyclized 471 xanthommatin because they were recently described [ (Figon and Casas, 2019) and this study], even 472 though the presence of uncyclized xanthommatin has been suspected (Bolognese and Scherillo, 1974). 473 Furthermore, a protocol to extract and purify ommochromasomes from housefly eyes is available 474 (Cölln et al, 1981), thus we can address the question of the localization of the metabolites from the 475 tryptophan ommochrome pathway.…”

“…How ommatins and ommins, the two most abundant families of ommochromes, are 632 biochemically connected to each other is still a mystery (Figon and Casas, 2019). Purple ommins have 633 higher molecular weights than ommatins and derive from both 3-hydroxykynurenine and cysteine/methionine, the latter providing sulfur to the phenothiazine ring of ommins (Linzen, 1974;635 Needham, 1974).…”

Pigmentation loci as markers for genome editing in the Chagas disease vector Rhodnius prolixus

“…aaNAT, with reported roles in pigment pattern of O. fasciatus [7] and Bombyx mori [19], encodes the central enzyme that generates unpigmented NADA sclerotin (arylalkylamine-Nacetyltransferase) ( Fig 1A). In insects, eye color requires the synthesis of ommochrome and pteridine pigments from tryptophan and guanine precursors, respectively, and their uptake into pigment granules by ABC transporters [10,20] (Fig 1B). vermillon (v), that encodes tryptophan oxidase, and cinnabar (cn, or kynu), that encodes kynurenin hydroxylase, are associated with the production of ommochromes [21][22][23][24].…”