Characterisation of protein families in spider digestive fluids and their role in extra-oral digestion

Abstract

BackgroundSpiders are predaceous arthropods that are capable of subduing and consuming relatively large prey items compared to their own body size. For this purpose, spiders have evolved potent venoms to immobilise prey and digestive fluids that break down nutrients inside the prey’s body by means of extra-oral digestion (EOD). Both secretions contain an array of active proteins, and an overlap of some components has been anecdotally reported, but not quantified. We systematically investigated the extent of such protein overlap. As venom injection and EOD succeed each other, we further infer functional explanations, and, by comparing two spider species belonging to different clades, assess its adaptive significance for spider EOD in general.ResultsWe describe the protein composition of the digestive fluids of the mygalomorph Acanthoscurria geniculata and the araneomorph Stegodyphus mimosarum, in comparison with previously published data on a third spider species. We found a number of similar hydrolases being highly abundant in all three species. Among them, members of the family of astacin-like metalloproteases were particularly abundant. While the importance of these proteases in spider venom and digestive fluid was previously noted, we now highlight their widespread use across different spider taxa. Finally, we found species specific differences in the protein overlap between venom and digestive fluid, with the difference being significantly greater in S. mimosarum compared to A. geniculata.ConclusionsThe injection of venom precedes the injection with digestive fluid, and the overlap of proteins between venom and digestive fluid suggests an early involvement in EOD. Species specific differences in the overlap may reflect differences in ecology between our two study species. The protein composition of the digestive fluid of all the three species we compared is highly similar, suggesting that the cocktail of enzymes is highly conserved and adapted to spider EOD.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-017-3987-9) contains supplementary material, which is available to authorized users.

Venomics of the ectoparasitoid wasp Bracon nigricans

“…However, the role of lysosomal alpha-mannosidase (LAM) and, more in general, the role of carbohydrases in entomophagous insects has been poorly characterized. LAMs, as well as the abovementioned trypsin-like serine protease and leucyl-cystinil aminopeptidase, are present in the digestive fluids of entomophagous arachnids (scorpions and spiders), which feed on their insect preys through extra-oral digestion (EOD) [95][96][97]. Enzymatic digestion through the action of saliva and digestive fluids represents a common strategy adopted by predatory arthropods and parasitoid wasps to exploit nutritional resources [98,99].…”

Polypeptides secreted from the columnar vesicles of the sea anemone Bunodosoma cangicum and their in vivo effects on Caenorhabditis elegans

“…The venom of some species of spiders such as Nephilengys cruentata show a similar effect, they secrete venom and intestinal fluids to both immobilize the prey and commence the digestive processes. Soon after, they ingest this liquid concoction of the dissolved prey (Foelix, 1983;Walter et al, 2017). This special capacity in spiders is of course, involved in their feeding processes, which is apparently different in purpose than the toxins shown here.…”

Not so Dangerous After All? Venom Composition and Potency of the Pholcid (Daddy Long-Leg) Spider Physocyclus mexicanus

“…Astacin-like metalloproteinases have also been detected as major components in digestive fluids secreted from the mouths of the mygalomorph Acanthoscurria geniculata (Walter et al, 2017) and araneomorphs Stegodyphus mimosarum (Walter et al, 2017), Nephilengys cruentata (Fuzita et al, 2016), and Argiope aurantia (Foradori et al, 2006) indicating a phylogenetically widespread presence in spider digestate. We are confident that the homologs we detect in venom proteomes represent presence in venom rather than contamination by regurgitate, because our venom collection techniques carefully exclude digestate.…”