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Venom Profiling of a Population of the Theraphosid Spider Phlogius

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Venom Profiling of a Population of the Theraphosid Spider Phlogius toxins Article Venom Profiling of a Population of the Theraphosid Spider Phlogius crassipes Reveals Continuous Ontogenetic Changes from Juveniles through Adulthood Renan C. Santana 1,2, David Perez 1, James Dobson 1, Nadya Panagides 1, Robert J. Raven 2, Amanda Nouwens 3, Alun Jones 4, Glenn F. King 4 and Bryan G. Fry 1,* 1 Venom Evolution Lab, School of Biological Sciences, University of Queensland, St Lucia, QLD 4072, Australia; [email protected] (R.C.S.); [email protected] (D.P.); [email protected] (J.D.); [email protected] (N.P.) 2 Terrestrial Biodiversity, Queensland Museum, South Brisbane BC, QLD 4101, Australia; [email protected] 3 School of Chemistry and Molecular Biology, University of Queensland, St Lucia, QLD 4072, Australia; [email protected] 4 Institute for Molecular Bioscience, University of Queensland, St Lucia, QLD 4072, Australia; [email protected] (A.J.); [email protected] (G.F.K.) * Correspondence: [email protected]; Tel.: +61-400-193-182 Academic Editor: Lourival D. Possani Received: 3 February 2017; Accepted: 5 March 2017; Published: 25 March 2017 Abstract: Theraphosid spiders (tarantulas) are venomous arthropods found in most tropical and subtropical regions of the world. Tarantula venoms are a complex cocktail of toxins with potential use as pharmacological tools, drugs and bioinsecticides. Although numerous toxins have been isolated from tarantula venoms, little research has been carried out on the venom of Australian tarantulas. We therefore investigated the venom profile of the Australian theraphosid spider Phlogius crassipes and examined whether there are ontogenetic changes in venom composition. Spiders were divided into four ontogenic groups according to cephalothorax length, then the venom composition of each group was examined using gel electrophoresis and mass spectrometry. We found that the venom of P. crassipes changes continuously during development and throughout adulthood. Our data highlight the need to investigate the venom of organisms over the course of their lives to uncover and understand the changing functions of venom and the full range of toxins expressed. This in turn should lead to a deeper understanding of the organism’s ecology and enhance the potential for biodiscovery. Keywords: tarantula; toxins; proteomic; mass spectrometry; LC/MS-MS; age 1. Introduction Spiders are abundant generalist predators that provide effective population control of other arthropods, most notably phytophagous insects [1]. They are found worldwide in all terrestrial ecosystems, except Antarctica. Araneae (Arthropoda: Arachnida) is one of the most speciose animal orders in the world [2], with >46,000 species, encompassing 4029 genera and 113 families [3]. Araneae is divided into two suborders, Mesothelae and Opisthothelae, with the latter suborder further subdivided into the infraorders Mygalomorphae and Araneomorphae. Mygalomorph spiders, known as primitive spiders, have two pairs of book lungs and a pair of parallel downward-facing chelicerae, each containing venom glands [4]. Toxins 2017, 9, 116; doi:10.3390/toxins9040116 www.mdpi.com/journal/toxins Toxins 2017, 9, 116 2 of 13 Theraphosidae is the most speciose mygalomorph family, with 140 genera encompassing 983 species [3]. Commonly known as tarantulas, bird-eating spiders, whistling or barking spiders, theraphosid spiders are the largest spiders in the world [5]. Like almost all spiders, they possess venom glands [6]. The main function of spider venom is prey acquisition, with predator deterrence as a secondary function [7–9]. Tarantula envenomations typically cause only mild symptoms in humans. However, species of the genera Latrodectus, Loxosceles, Phoneutria, Atrax, Illawarra and Hadronyche can cause sickness and even death [10,11]. Spider venom is a complex cocktail of different molecules including inorganic salts, small molecules such as amino acids, neurotransmitters and larger polyamines, peptides, and proteins [7–9]. The different compounds in spider venom are thought to work synergistically, thus increasing venom efficiency [9,12,13]. It has been estimated that each spider venom contains more than 100 peptides, with some containing more than 1000, which provides an immense natural pharmacopeia [10]. Spider venom composition may be influenced by different predatory niche factors such as sex, diet, habitat and climate, making the venom possibly species-specific and enlarging the opportunity for drug discovery [9]. Early studies of spider venoms focused on medically important spiders with a view towards development of antivenom [10]. Since the turn of the century, our increased understanding of the molecular composition of spider venoms and the mode of action of spider-venom compounds has led to the development of spider-venom peptides as pharmacological tools, drugs and bioinsecticides [14–17]. The venom ontogeny of spiders has been studied in species of the infraorder Araneomorphae, with a focus on differences related to size, sex and defense behaviour [18–21]. In contrast, although differences in venom composition between sexes have been investigated in mygalomorphs using modern molecular tools, ontogenetic variation in venom has only been studied using differences in LD50 and venom yield [22–24]. In other studies, focusing on different aspects of venom, ontogenetic variation in venom composition was only reported on briefly [25,26]. Thus, this study aims to provide, for the first time, a full venom proteomics characterization of ontogenetic variation within a population of mygalomorph spiders, namely the Australian tarantula Phlogius crassipes [27]. 2. Results 2.1. LC-MS Analysis of Venom LC-MS analysis of tarantula venoms was performed to provide a visual means of comparing the variation in venom composition between size groups. Peaks in the chromatogram correspond to the detection of a toxin or group of toxins with similar hydrophobicity. However, this method does not provide a comprehensive overview of venom complexity as most LC peaks will be comprised of multiple toxins. Both extreme size groups showed a smaller number of peaks (Olkola extra small (OXS) and Olkola large (OL) with 9 peaks) (Figure1a,d) compared with the intermediate groups (Olkola small (OS) and Olkola medium (OM) with 11 peaks) (Figure1b,c). Small variations in intensity were noted in all chromatograms, but could be due to individual variation. Clear differences in peaks were observed between the smallest (Figure1a) and largest (Figure1d) groups while the intermediate groups (Figure1b,c) did not differ significantly. Group OXS lacks the peaks around 7, 14, and 18 min that are observed in chromatograms from all other groups. Also, the OXS group has peaks of lower intensity at 10 and 15 min compared to its closest group (OS). Group OL lacks the peaks at 13, 28 and 30 min that are present in chromatograms from all other groups and it differs in the intensity of peaks at 15 and 21 min. Principal component analysis and discriminant analysis (PCA-DA) (95.5%) showed a pattern of change in venom according to spider size (Figure2), with gradual changes in venom pattern. However, it is clear that the venoms from tarantulas smaller than 10 mm (OXS) are different from tarantulas bigger than 10.1 mm (OS, OM and OL). Although specimens from the OS and OM groups are mixed in Toxins 2017, 9, 116 3 of 13 the central area of PCA-DA graph, OS spiders are more close to OXS spiders, while OM spiders are closer to OL. Adult tarantulas bigger than 15.5 mm (group OL) are dispersed over a larger area of the graph, but they overlap with OM in a small region. Time, min (a ) Time, min (b) 1 Time, min (c) Figure 1. Cont. 2 Toxins 2017, 9, 116 5 of 15 Toxins 2017, 9, 116 4 of 13 Time, min (d) FigureFigure 1. Combined 1. Combined liquid chromatography liquid chromatography (LC) chromatograms (LC) chromatograms of specimens from of specimensthe (a) OXS from– Olkola the extra small(a) OXS group, – Olkola (b) OS extra – Olkola small group,small group, (b) OS ( –c) Olkola OM – Olkola small group, medium (c) group, OM – Olkola and (d medium) OL – Olkola group, large and group.(d Each) OL –colour Olkola represent large group. a different Each colour specimen. represent Vertical a different axis is specimen.Intensity and Vertical horizontal axis is Intensityaxis is Time and (minuteshorizontal). axis is Time (minutes). 3 Figure 2. Principal component analysis and discriminant analysis (PCA-DA) analysis of Phlogius Figurecrassipes 2.population Principal component from Olkola analysis Aboriginal and land. discriminant Tarantulas analysis are grouped (PCA according-DA) analysis to cephalothorax of Phlogius crassipessize. Each population dot represents from Olkola a specimen. Aboriginal land. Tarantulas are grouped according to cephalothorax size. Each dot represents a specimen. 2.2. Shotgun Sequencing of Venom Peptides and Proteins LC-MS/MS of whole venoms (shotgun) was conducted to identify toxins found in each size group and determine if any changes in venom were occurring over the lifespan of P. crassipes. For a small number of spiders, it was difficult to extract a significant amount of venom. This was especially true for smaller specimens from the OXS and OS groups, which limited sample numbers for some analyses. Toxins 2017, 9, 116 5 of 13 The individuals selected to perform the shotgun analyses followed by LC-MS/MS were representative of each group. MS analysis revealed a total of 12 peptides/proteins in the OXS group, 11 in OS, 8 in OM and 8 in OL. These results contrast with the LC/MS data presented above that showed more complexity in the venoms of OS and OM spiders (11 peaks), and less complexity in venom from OXS and OL spiders (9 peaks). However, as the LC/MS peaks can have one or more toxins with similar hydrophobicity overlapping in the chromatogram, the venom can be more complex in the early stages of life of tarantulas. On the other hand, the lack of a comprehensive database to match all the toxins in the venom may be responsible for the non-corroborative results between the shotgun and LC/MS analyses.
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