Roles of biogenic amines in regulating bioluminescence in the Australian glowworm Arachnocampa flava

Abstract

SUMMARY The glowworm Arachnocampa flava is a carnivorous fly larva (Diptera) that uses light to attract prey into its web. The light organ is derived from cells of the Malpighian tubules, representing a bioluminescence system that is unique to the genus. Bioluminescence is modulated through the night although light levels change quite slowly compared with the flashing of the better-known fireflies (Coleoptera). The existing model for the neural regulation of bioluminescence in Arachnocampa, based on use of anaesthetics and ligations, is that bioluminescence is actively repressed during the non-glowing phase and the repression is partially released during the bioluminescence phase. The effect of the anaesthetic, carbon dioxide, on the isolated light organ from the present study indicates that the repression is at least partially mediated at the light organ itself rather than less directly through the central nervous system. Blocking of neural signals from the central nervous system through ligation leads to uncontrolled release of bioluminescence but light is emitted at relatively low levels compared with under anaesthesia. Candidate biogenic amines were introduced by several methods: feeding prey items injected with test solution, injecting the whole larva, injecting a ligated section containing the light organ or bathing the isolated light organ in test solution. Using these methods, dopamine, serotonin and tyramine do not affect bioluminescence output. Exposure to elevated levels of octopamine via feeding, injection or bathing of the isolated light organ indicates that it is involved in the regulation of repression. Administration of the octopamine antagonists phentolamine or mianserin results in very high bioluminescence output levels, similar to the effect of anaesthetics, but only mianserin acts directly on the light organ.

Molecular, pharmacological, and signaling properties of octopamine receptors from honeybee (Apis mellifera) brain

“…; Kaczer and Maldonado ; Mizunami et al . ; Rigby and Merritt ; Rillich et al . ) were performed to uncover the functional role of biogenic amines in these animals.…”

“…In vivo pharmacological studies in honeybees (e.g., Braun and Bicker 1992;Pribbenow and Erber 1996;Menzel et al 1999;Scheiner et al 2002;Farooqui et al 2003) and other arthropods (e.g., Zornik et al 1999;Kaczer and Maldonado 2009;Mizunami et al 2009;Rigby and Merritt 2011;Rillich et al 2011) were performed to uncover the functional role of biogenic amines in these animals. These approaches, however, suffered from some caveats because the number of proteins constituting the receptor families as well as the pharmacological properties and intracellular signaling mechanisms of individual receptors were not precisely known.…”

Trace Amines and Their Receptors

“…OCT-mediated regulation of immune responses (Huang et al, 2012) and a role in reproductive behavior have also been reported (Lee et al, 2003;Lim et al, 2014). In the firefly, OCT is well established to underlie the neural basis of light emission (Copeland and Robertson, 1982;Christensen et al, 1983;Hashemzadeh et al, 1985) and also regulates bioluminescent emissions in glow worms (Rigby and Merritt, 2011). Modulation of sensory inputs by OCT is also well established (Farooqui, 2007), with effects seen in relation to vision (Bacon et al, 1995;Scheiner et al, 2014), olfaction (Barron et al, 2002;Anton et al, 2006;Farooqui, 2007;Flecke and Stengl, 2009;Cassenaer and Laurent, 2012;Ma et al, 2015), hearing (Andrés et al, 2016), taste (Scheiner et al, 2002;Pankiw and Page, 2003), and touch and proprioception (Büschges et al, 1993;Skorupski, 1996).…”

The Carbon Dioxide-induced Bioluminescence Increase inArachnocampaLarvae

“…The photocytes have a dense cytoplasm with synaptic contacts on the cells of the light organ containing dense-core vesicles that are indicative of neurosecretory regulation (Green, 1979). A single nerve runs from the terminal abdominal ganglion (TAG), separating into neural processes that innervate the LO (Gatenby, 1959; Rigby and Merritt, 2011). The lateral and ventral surfaces of the LO are covered by a mass of tracheoles with interspersed nuclei, taking on a silvery appearance visible through the cuticle (Green, 1979; Rigby and Merritt, 2011).…”

“…A single nerve runs from the terminal abdominal ganglion (TAG), separating into neural processes that innervate the LO (Gatenby, 1959; Rigby and Merritt, 2011). The lateral and ventral surfaces of the LO are covered by a mass of tracheoles with interspersed nuclei, taking on a silvery appearance visible through the cuticle (Green, 1979; Rigby and Merritt, 2011). The tracheal layer is closely associated with the photocytes (Green, 1979), suggesting that access to oxygen is a critical factor in bioluminescence output just as it is in fireflies (Ghiradella and Schmidt, 2004); however, the firefly LO is evolutionary derived from a different tissue, believed to be fat body (Amaral et al, 2017).…”