A transcriptional and proteomic survey of Arachnocampa luminosa (Diptera: Keroplatidae) lanterns gives insights into the origin of bioluminescence from the Malpighian tubules in Diptera

Abstract

Fungus-gnats of the genus Arachnocampa are unique among bioluminescent insects for displaying blue-green bioluminescence, and are responsible for one of the most beautiful bioluminescence spectacles on the roofs of the Waitomo Caves. Despite morphological studies showing that Arachnocampa larval lanterns involve specialization of the Malpighian tubules, the biochemical origin of their bioluminescence remains enigmatic. Using a cDNA library previously constructed from lanterns of the New Zealand glowworm A. luminosa, we carried out the first transcriptional analysis of ~ 500 expressed sequence tags (ESTs) to identify putative candidate proteins for light production, and to better understand the molecular physiology of the lanterns and their relationship with Malpighian tubule physiology. The analysis showed an abundance of hexamerin-like proteins, as well as luciferase-like enzymes, indicating a possible critical role for these proteins in bioluminescence. These findings were corroborated by proteomic analysis of lantern extracts, which showed the presence of hexamerins and luciferase-like enzymes. Other gene products typical of Malpighian tubules, such as detoxifying enzymes, were also found. The results support the existence of an evolutionary link between Malpighian tubule detoxification and the origin of bioluminescence in these Diptera.

Comparative Evolution of Sand Fly Salivary Protein Families and Implications for Biomarkers of Vector Exposure and Salivary Vaccine Candidates

“…Amongst the salivary gene families unique to NW sand flies, the c-type lectin, the mannose-binding lectin, and the spider toxin-like gene families share paralogs expressed in other tissues of sand flies and other unrelated arthropods (Abdeladhim et al, 2016). Similar phenomena were noticed for salivary protein families unique to OW sand flies, such as phospholipase A2 (Tunaz et al, 2003) and pyrophosphatase (Silva et al, 2015), as well as in protein families shared with NW sand flies, like hyaluronidase (Allalouf et al, 1975), endonuclease (Broderick et al, 2014), adenosine deaminase (Dolezelova et al, 2005), and OBPs (Benoit et al, 2017). Hence, such gene families seem to have emerged by sub-functionalization.…”

Know your insect: Malpighian tubules in Trichoplusia ni (Lepidoptera: Noctuidae)

“…Malpighian tubules are also capable of secreting silk-like substances. This 'malpighian silk' has been observed in Neuroptera, Coleoptera and Hymenoptera [Sutherland et al 2010]. Also, Eguileor et al (2001) has suggested that salivary glands in the aphid parasitoid Aphidius ervi might be functioning as an excretory tissue.…”

“…With the explosion of high throughput techniques, the transcriptome, proteome and even metabolome of Malpighian tubules from several species are being characterized [Esquivel et al 2014, Silva et al 2015, Dow and Davies 2006, Zhong et al 2013. These characterizations are consistently identifying molecules involved in detoxification as well as immunity.…”

“…The glowing that attracts so many tourists comes from Arachnocampa luminosa commonly known as the New Zealand glowworm. These are fungus gnats, which produce a bioluminescent substance in their Malpighian tubules [Silva et al 2015]. The reaction and specific compounds involved in this bioluminescence are not fully understood but regardless, it makes for a beautiful spectacle.…”

Comparative physiology of Malpighian tubules: form and function

“…11,27 Genomic and proteomic analysis studies may elucidate their intracellular signaling mechanisms, 81,82 regulating the immune response, 83 in addition to other functions of MTs, as their relationship with the bioluminescence mechanism in some insects. 84,85 The results indicate that MTs can be used for the evaluation of biomarkers, at the cellular level, in toxicological studies, especially studies done with sublethal doses and concentrations of chemicals. The various roles played by MTs reflect the interactions that organisms have with the environment in which they live.…”