Characterization of an anthraquinone fluor from the bioluminescent, pelagic polychaete Tomopteris

Abstract

Tomopteris is a cosmopolitan genus of polychaetes. Many species produce yellow luminescence in the parapodia when stimulated. Yellow bioluminescence is rare in the ocean and the components of this luminescent reaction have not been identified. Only a brief description half a century ago noted a fluorescence in the parapodia with a remarkably similar spectrum to the bioluminescence, which suggested that it may be the luciferin or terminal light-emitter. Here we report the isolation of the fluorescent yellow-orange pigment found in the luminous exudate and in the body of the animals. LCMS revealed the mass to be 270m/z with a molecular formula of C15H10O5, which ultimately was shown to be aloe-emodin, an anthraquinone previously found in plants. We speculate that aloe-emodin could be a factor for resonant-energy transfer or the oxyluciferin for Tomopteris bioluminescence.

Behavioural responses of the yellow emitting annelid Tomopteris helgolandica to photic stimuli

“…The temporal dynamics was similar to the monophasic response induced in this species by 200 mM KCl or 10 mM carbachol. [15] The emission of T. helgolandica is not secreted in contrast to what was observed in other Tomopteris species [31,48] and it was not responsive to photic stimulation according to our low-light-level video recordings.…”

“…That being said, bioluminescent may act in a variety of ways as suggested by the recently evidenced diversity of emission patterns of tomopterid species . The light emission of T. helgolandica , intracoelomic according to Meyer and as recently supported by histological observations, could induce a startle effect while the secreted luminescence of Tomopteris carpenteri Quatrefages, 1866 and other species would rather act as a smoke screen confusing the predator while the worm escapes. Also, the production of mucus, depending on the chemical properties and on whether the light and mucus production are associated, might act as an aposematic function.…”

Insights into the Biodiversity, Behavior, and Bioluminescence of Deep-Sea Organisms Using Molecular and Maritime Technology

“…Free-swimming polychaetes of the genus Tomopteris are some of the very few marine organisms that produce yellow light Francis et al, 2016b). The chemistry of the light-emitter (luciferin) in this system is as yet unknown, but the chemical composition of the yellow fluorescent compound (not necessarily luminescent) has been determined in the worms (Francis et al, 2014). This molecule is likely involved in the luminescence reaction and could ultimately provide a novel biotechnological tool.…”

“…Today, ultra-high-performance liquid chromatography (UHPLC) allows isolation of proteins and other substances from small amounts of starting material; this led to the isolation and purification of the yellow fluorescent compound that may give the worm Tomopteris its unique bioluminescence spectrum (Figure 9; Francis et al, 2014). These isolates can be used to locate the associated gene, which can then be inserted into bacteria to fabricate large amounts of protein for characterization.…”

Bioluminescence properties of Thelepus japonicus (Annelida: Terebelliformia)

“…The scaleworm's photoprotein, polynoidin, was purified from Harmothoe . The involvement of an anthraquinone, aloe‐emodin, in the bioluminescence of a deep‐sea planktonic worm Tomopteris , and riboflavin‐like compound, photoprotein and ferritin in the bioluminescence of a parchment tubeworm Chaetopterus have been reported. Conversely, studies into bioluminescence systems of other annelids have been very limited, especially for Terebelliformia, which is one of the groups least studied for its bioluminescence properties, along with Flabelligeridae, Onuphidae and Cirratulidae …”